Marcel Visser

Prof. dr. Marcel Visser

Afdelingshoofd

Bezoekadres

Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands

Over

The Visser-group provided strong empirical evidence that species are responding to recent anthropogenic climate change. Species however shift their seasonal timing (or phenology) at different rates. This disrupts the temporal synchrony between species.

Biografie

Marcel Visser is widely recognized as a world-leading expert on the ecological and evolutionary impact of anthropogenic environmental changes. He aims to understand how climate change disrupts natural systems, using long-term studies on wild species. His work on phenological mismatch within food chains has turned his model species, the great tit, into the poster child for climate change impact. In his research he integrates work on epigenetic regulation of gene expression, fitness consequences of timing in the wild, with the impact of climate-change on population numbers. 

Visser is involved in a wide range of projects, including bringing together long-term data on populations of individually known birds (SPI-Birds) to make such data FAIR, and more recently he has taken the lead in using data from Long-Term Ecosystem Research sites in the Netherlands (LTER-NL). 

Recently, he has taken up a leading role in building a Large-Scale Research Infrastructure named LTER-LIFE. LTER-LIFE aims to provide researchers with the tools to build so-called Digital Twins of entire ecosystems, starting with the Veluwe en the Wadden sea ecosystems. These Digital Twins will be used to better understand the functioning of ecosystems and to carry out scenario studies that can be used to forecast the effects of different climate change scenarios or the impact of mitigation measures, such as nitrogen reduction. The project has started in August 2023 and is funded for the first 10 years by NWO.

Together, these research lines show Visser’s unique strength to bring people together around the crucial next question and sets-up targeted, large-scale experiments that advances the field; working in the wild, under controlled conditions and in the molecular laboratory.

Visser has been awarded a NWO-VICI and an ERC Advanced grant, and has been elected as a member of the Royal Netherlands Academy of Sciences (KNAW). He is co-founder and inaugural president of the Netherlands Society for Evolutionary Biology (NLSEB). Prof Visser has published 252 papers, resulting in an h-index of 71 and >19500 citations making him a Publons Highly Cited Researcher.

Onderzoeksgroepen

CV

Nevenfuncties

Publicaties

Peer-reviewed publicaties

  • Evolution Letters
    06-03-2025

    Size in the city

    Barbara Tomotani, Mika Couweleers, Bram ten Brinke, Anne Walboom, Kees van Oers, Marcel E. Visser
    Animals living in cities are smaller than their conspecifics from rural areas but whether such differences are caused by genetic differences or food constraints remains untested. We performed a multi-generation common garden study where we raised great tits (Parus major), originating from eggs collected from multiple Dutch cities and forests under the same conditions for two generations. Offspring from city birds had a smaller tarsus than forest birds in both generations, demonstrating that these morphological differences are genetic. Next, we tested whether size differences are an adaptation to the low food abundance when offspring are raised in the city. Third-generation birds of both origins were given food amounts mimicking being raised in forests or cities during the second part of their nestling development. While the treatment resulted in birds in the lower feeding frequency treatment to be smaller, city and forest birds responded the same way, suggesting that city birds do not cope better with reduced food availability. Our study shows that the smaller size of urban birds has a genetic basis and is not only caused by a plastic response to restricted resources in the urban environment. Our experiment does not provide evidence that these genetic differences have evolved as an adaptive response to a reduced food availability in cities.
    https://doi.org/10.1093/evlett/qraf006
  • Ecology Letters
    02-2025

    Continent-Wide Drivers of Spatial Synchrony in Breeding Demographic Structure Across Wild Great Tit Populations

    Joe P. Woodman, Stefan Vriend, Frank Adriaensen, Elena Álvarez, Alexander V. Artemyev, Emilio Barba, Malcolm D. Burgess, Samuel P. Caro, Laure Cauchard, Anne Charmantier, Ella F. Cole, Niels Dingemanse, Blandine F. Doligez, Tapio Eeva, Simon R. Evans, Arnaud Grégoire, Marcel M. Lambrechts, Agu Leivits, András Liker, Erik Matthysen, Markku Orell, John S. Park, Seppo Rytkönen, Juan Carlos Senar, Gábor Seress, Marta Szulkin, Kees van Oers, Emma Vatka, Marcel E. Visser, Josh A. Firth, Ben C. Sheldon

    Variation in age structure influences population dynamics, yet we have limited understanding of the spatial scale at which its fluctuations are synchronised between populations. Using 32 great tit populations, spanning 4° W–33° E and 35°–65° N involving > 130,000 birds across 67 years, we quantify spatial synchrony in breeding demographic structure (subadult vs. adult breeders) and its drivers. We show that larger clutch sizes, colder winters, and larger beech crops lead to younger populations. We report distance-dependent synchrony of demographic structure, maintained at approximately 650 km. Despite covariation with demographic structure, we do not find evidence for environmental variables influencing the scale of synchrony, except for beech masting. We suggest that local ecological and density-dependent dynamics impact how environmental variation interacts with demographic structure, influencing estimates of the environment's effect on synchrony. Our analyses demonstrate the operation of synchrony in demographic structure over large scales, with implications for age-dependent demography in populations.

    https://doi.org/10.1111/ele.70079
  • Proceedings of the Royal Society B: Biological Sciences
    29-01-2025

    Geographic differences in the phenology of gonadal development and moult, but not of egg laying, are genetically based in a small songbird

    Marcel E. Visser, Kees van Oers, Anne Charmantier, Szymon M. Drobniak, Carys Jones, Erik Mathyssen, Melissah Rowe, Barbara Tomotani
    To forecast how fast populations can adapt to climate change, it is essential to determine the evolutionary potential of different life-cycle stages under selection. In birds, timing of gonadal development and moult are primarily regulated by photoperiod, while laying date is highly phenotypically plastic to temperature. We tested whether geographic variation in phenology of these life-cycle events between populations of great tits (Parus major) has a genetic basis, indicating that contemporary genetic adaptation is possible. We carried out a common garden experiment in which we bred first- and second-generation pairs in captivity originating from eggs from Gotland (Sweden) and Hoge Veluwe (The Netherlands), two populations that showed different temperature sensitivity of laying date in a recent meta-analysis. We recorded the phenology of egg-laying, moult and gonadal size in early spring. We found no significant differences in laying date between the populations, but they did differ in moult timing and testis size. This implies that under climate change the timing of gonadal development and moult, which are mainly regulated by photoperiod, will not respond to increased temperature but can respond by genetic adaptation in response to selection, while the opposite holds for laying date, perhaps indicating that plasticity is constraining genetic adaptation.
    https://doi.org/10.1098/rspb.2024.2286
  • Science of the Total Environment
    25-08-2024

    Artificial light at night drives diel activity patterns of synanthropic pipistrelle bats and their prey

    Claire Hermans, Iryna Litovska, Mélyssa De Pastors, Marcel E. Visser, Kamiel Spoelstra
    The use of artificial light at night (ALAN) has increased drastically worldwide over the last decades. ALAN can have major effects on nocturnal communities, including insects and bats. Insects are attracted to street lights and few bat species take advantage of this by foraging on the attracted insects. ALAN potentially affects the temporal patterns of insect abundance and thereby bat foraging behaviour. In a natural dark environment, these patterns are usually bimodal, with an activity peak in the early evening and the morning. Little is known about how ALAN affects insect presence throughout the night, and whether the light spectrum plays a role. This is important, as these temporal changes may be a key driver of disturbances in bat-insect interactions. Here, we studied how white and red light affect insects' and bats' nightly activity patterns. The activity of insects and bats (Pipistrellus spp.) was recorded throughout the night at seven experimentally illuminated sites in a forest-edge ecosystem. ALAN disrupted activity patterns, with both insects and bats being more active throughout the night. ALAN facilitated all-night foraging in bats especially near white light, but these effects were attenuated near red light. The ability to forage throughout the night may be a key advantage causing synanthropic bats to dominate in illuminated environments, but this could also prove detrimental in the long term. As red light reduced disturbing effects of ALAN on insects and bats diel activity pattern, it opens the possibility of using spectral composition as a mitigation measure.
    https://doi.org/10.1016/j.scitotenv.2024.173699
  • Biology Letters
    03-07-2024

    Revisiting Perdeck's massive avian migration experiments debunks alternative social interpretations

    Morrison Pot, Marcel E. Visser, Barbara Helm, Jan A. C. von Rönn, Henk P. van der Jeugd
    Whether avian migrants can adapt to their changing world depends on the relative importance of genetic and environmental variation for the timing and direction of migration. In the classic series of field experiments on avian migration, A. C. Perdeck discovered that translocated juveniles failed to reach goal areas, whereas translocated adults performed ‘true-goal navigation’. His translocations of > 14 000 common starlings (Sturnus vulgaris) suggested that genetic mechanisms guide juveniles into a population-specific direction, i.e. ‘vector navigation’. However, alternative explanations involving social learning after release in juveniles could not be excluded. By adding historical data from translocation sites, data that was unavailable in Perdeck's days, and by integrated analyses including the original data, we could not explain juvenile migrations from possible social information upon release. Despite their highly social behaviour, our findings are consistent with the idea that juvenile starlings follow inherited information and independently reach their winter quarters. Similar to more solitarily migrating songbirds, starlings would require genetic change to adjust the migration route in response to global change.
    https://doi.org/10.1098/rsbl.2024.0217
  • Molecular Ecology Resources
    07-2024

    The great tit HapMap project

    Lewis G. Spurgin, Mirte Bosse, Frank Adriaensen, Tamer Albayrak, Christos Barboutis, Eduardo Belda, Andrey Bushuev, Jacopo G. Cecere, Anne Charmantier, Mariusz Cichoń, N.J. Dingemanse, Blandine F. Doligez, Tapio Eeva, Kjell Einar Erikstad, Vyacheslav Fedorov, Matteo Griggio, Dieter Heylen, Sabine Hille, C.A. Hinde, Elena V. Ivankina, Bart Kempenaers, Anvar B. Kerimov, Miloš Krist, Laura Kvist, Veronika Laine, Raivo Mänd, Erik Matthysen, Ruedi G. Nager, Boris P. Nikolov, Ana C. Norte, Markku Orell, Jenny Ouyang, Gergana Petrova-Dinkova, Heinz Richner, Diego Rubolini, Tore Slagsvold, Vallo Tilgar, János Török, Barbara Tschirren, Csongor I. Vágási, Teru Yuta, Martien A.M. Groenen, Marcel E. Visser, Kees van Oers, Ben C. Sheldon, Jon Slate

    A major aim of evolutionary biology is to understand why patterns of genomic diversity vary within taxa and space. Large-scale genomic studies of widespread species are useful for studying how environment and demography shape patterns of genomic divergence. Here, we describe one of the most geographically comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit (Parus major) HapMap project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning ~30 degrees of latitude and 40 degrees of longitude – almost the entire geographical range of the European subspecies. Genome-wide variation was consistent with a recent colonisation across Europe from a South-East European refugium, with bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly heterogeneous, with clear ‘islands of differentiation’, even among populations with very low levels of genome-wide differentiation. Low local recombination rates were a strong predictor of high local genomic differentiation (FST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination causes highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, probably as a result of recent directional selection at the species' range edges. Haplotype-based measures of selection were related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into spatio-temporal evolutionary dynamics.

    https://doi.org/10.1111/1755-0998.13969
  • Evolutionary Applications
    07-2024

    Genetic and epigenetic differentiation in response to genomic selection for avian lay date

    Melanie Lindner, Irene C. Verhagen, A.C. Mateman, Kees van Oers, Veronika Laine, Marcel E. Visser
    Anthropogenic climate change has led to globally increasing temperatures at an unprecedented pace and, to persist, wild species have to adapt to their changing world. We, however, often fail to derive reliable predictions of species' adaptive potential. Genomic selection represents a powerful tool to investigate the adaptive potential of a species, but constitutes a ‘blind process’ with regard to the underlying genomic architecture of the relevant phenotypes. Here, we used great tit (Parus major) females from a genomic selection experiment for avian lay date to zoom into this blind process. We aimed to identify the genetic variants that responded to genomic selection and epigenetic variants that accompanied this response and, this way, might reflect heritable genetic variation at the epigenetic level. We applied whole genome bisulfite sequencing to blood samples of individual great tit females from the third generation of bidirectional genomic selection lines for early and late lay date. Genomic selection resulted in differences at both the genetic and epigenetic level. Genetic variants that showed signatures of selection were located within genes mostly linked to brain development and functioning, including LOC107203824 (SOX3-like). SOX3 is a transcription factor that is required for normal hypothalamo-pituitary axis development and functioning, an essential part of the reproductive axis. As for epigenetic differentiation, the early selection line showed hypomethylation relative to the late selection line. Sites with differential DNA methylation were located in genes important for various biological processes, including gonadal functioning (e.g., MSTN and PIK3CB). Overall, genomic selection for avian lay date provided insights into where within the genome the heritable genetic variation for lay date, on which selection can operate, resides and indicates that some of this variation might be reflected by epigenetic variants.
    https://doi.org/10.1111/eva.13703
  • Hormones and Behavior
    01-04-2024

    Odours of caterpillar-infested trees increase testosterone concentrations in male great tits

    Ségolène Delaitre, Marcel E. Visser, Kees van Oers, Samuel P. Caro
    Trees release Herbivore-Induced Plant Volatiles (HIPVs) into the air in response to damage inflicted by insects. It is known that songbirds use those compounds to locate their prey, but more recently the idea emerged that songbirds could also use those odours as cues in their reproductive decisions, as early spring HIPVs may contain information about the seasonal timing and abundance of insects. We exposed pre-breeding great tits (Parus major) to the odours of caterpillar-infested trees under controlled conditions, and monitored reproduction (timing of egg laying, number of eggs, egg size) and two of its main hormonal drivers (testosterone and 17β-estradiol in males and females, respectively). We found that females exposed to HIPVs did not advance their laying dates, nor laid larger clutches, or larger eggs compared to control females. 17β-estradiol concentrations in females were also similar between experimental and control birds. However, males exposed to HIPVs had higher testosterone concentrations during the egg-laying period. Our study supports the hypothesis that insectivorous songbirds are able to detect minute amounts of plant odours. The sole manipulation of plant scents was not sufficient to lure females into a higher reproductive investment, but males increased their reproductive effort in response to a novel source of information for seasonal breeding birds.
    https://doi.org/10.1016/j.yhbeh.2024.105491
  • Oecologia
    23-03-2024

    Temperature has an overriding role compared to photoperiod in regulating the seasonal timing of winter moth egg hatching

    To accurately predict species’ phenology under climate change, we need to gain a detailed mechanistic understanding of how different environmental cues interact to produce the seasonal timing response. In the winter moth (Operophtera brumata), seasonal timing of egg hatching is strongly affected by ambient temperature and has been under strong climate change-induced selection over the past 25 years. However, it is unclear whether photoperiod received at the egg stage also influences timing of egg hatching. Here, we investigated the relative contribution of photoperiod and temperature in regulating winter moth egg development using two split-brood experiments. We experimentally shifted the photoperiod eggs received by 2–4 weeks compared to the actual calendar date and measured the timing of egg hatching, both at a constant temperature and in combination with two naturally changing temperature treatments – mimicking a cold and a warm year. We found an eight-fold larger effect of temperature compared to photoperiod on egg development time. Moreover, the very small photoperiod effects we found were outweighed by both between- and within-clutch variation in egg development time. Thus, we conclude that photoperiod received at the egg stage does likely not play a substantial role in regulating the seasonal timing of egg hatching in the winter moth. These insights into the regulatory mechanism of seasonal timing could have important implications for predicting insect climate change adaptation, as we might expect different targets of selection depending on the relative contribution of different environmental cues.
    https://doi.org/10.1007/s00442-024-05535-w
  • Journal of Experimental Zoology Part A: Ecological and Integrative Physiology
    08-02-2024

    Short-time exposure to light at night affects incubation patterns and correlates with subsequent body weight in great tits (Parus major)

    Aurelia Strauss, Lies Bosma, Marcel E. Visser, Barbara Helm

    Artificial light at night (ALAN) widely affects wildlife by blurring light-dark differences, including transitions such as sunrise and sunset, thereby affecting regulation of diel rhythms. As a result, activity onsets in many wild diurnal songbirds advance under ALAN. From chronobiological studies, it is known that the direction and strength of the response to light depends on when during the night exposure takes place. However, these experiments are mostly done under continuous light conditions, when animals have free-running rhythms. It remains unclear whether phase-dependence also holds in entrained, wild songbirds; i.e., does the effect of ALAN on activity patterns differ between exposure in the morning compared to the evening? This information is essential to assess the effects of mitigation measures by limiting ALAN to selected times of the night. We exposed incubating great tits (Parus major) inside the nest-box to 4 h of dim light, of which 1 h overlapped with dawn before sunrise or dusk after sunset. We found a small advancing effect of morning-light on activity onset and of evening-light on offset compared to dark controls but not vice versa. Breeding success and chick condition were unaffected by the light treatments. However, light-treated females had lower weights 9–18 days after the end of the treatment compared to the controls, independent of whether ALAN occurred in the morning or the evening, indicating possible costs of ALAN. Despite the weak behavioral response, ALAN might have affected the females' circadian clock or physiology resulting in lower body condition.

    https://doi.org/10.1002/jez.2787
  • Evolution Letters
    01-02-2024

    Divergence in evolutionary potential of life history traits among wild populations is predicted by differences in climatic conditions

    Stéphane Chantepie, Anne Charmantier, Boris Delahaie, Frank Adriaensen, Erik Matthysen, Marcel E. Visser, Elena Álvarez, Emilio Barba, Markku Orell, Ben C. Sheldon, Elena V. Ivankina, Anvar B. Kerimov, Sébastien Lavergne, Céline Teplitsky
    Short-term adaptive evolution represents one of the primary mechanisms allowing species to persist in the face of global change. Predicting the adaptive response at the species level requires reliable estimates of the evolutionary potential of traits involved in adaptive responses, as well as understanding how evolutionary potential varies across a species’ range. Theory suggests that spatial variation in the fitness landscape due to environmental variation will directly impact the evolutionary potential of traits. However, empirical evidence on the link between environmental variation and evolutionary potential across a species range in the wild is lacking. In this study, we estimate multivariate evolutionary potential (via the genetic variance–covariance matrix, or G-matrix) for six morphological and life history traits in 10 wild populations of great tits (Parus major) distributed across Europe. The G-matrix significantly varies in size, shape, and orientation across populations for both types of traits. For life history traits, the differences in G-matrix are larger when populations are more distant in their climatic niche. This suggests that local climates contribute to shaping the evolutionary potential of phenotypic traits that are strongly related to fitness. However, we found no difference in the overall evolutionary potential (i.e., G-matrix size) between populations closer to the core or the edge of the distribution area. This large-scale comparison of G-matrices across wild populations emphasizes that integrating variation in multivariate evolutionary potential is important to understand and predict species’ adaptive responses to new selective pressures.
    https://doi.org/10.1093/evlett/qrad067
  • Philosophical transactions of the Royal Society of London. Series B, Biological sciences
    18-12-2023

    Long-term exposure to experimental light affects the ground-dwelling invertebrate community, independent of light spectra

    Kamiel Spoelstra, Sven Teurlincx, Matthijs Courbois, Zoë M. Hopkins, Marcel E. Visser, Therésa M. Jones, Gareth R. Hopkins

    Our planet endures a progressive increase in artificial light at night (ALAN), which affects virtually all species, and thereby biodiversity. Mitigation strategies include reducing its intensity and duration, and the adjustment of light spectrum using modern light emitting diode (LED) light sources. Here, we studied ground-dwelling invertebrate (predominantly insects, arachnids, molluscs, millipedes, woodlice and worms) diversity and community composition after 3 or 4 years of continued nightly exposure (every night from sunset to sunrise) to experimental ALAN with three different spectra (white-, and green- and red-dominated light), as well as for a dark control, in natural forest-edge habitat. Diversity of pitfall-trapped ground-dwelling invertebrates, and the local contribution to beta diversity, did not differ between the dark control and illuminated sites, or between the different spectra. The invertebrate community composition, however, was significantly affected by the presence of light. Keeping lights off during single nights did show an immediate effect on the composition of trapped invertebrates compared to illuminated nights. These effects of light on species composition may impact ecosystems by cascading effects across the food web. This article is part of the theme issue 'Light pollution in complex ecological systems'.

    https://doi.org/10.1098/rstb.2022.0364
  • Proceedings of the Royal Society B: Biological Sciences
    18-10-2023

    Climate change does not equally affect temporal patterns of natural selection on reproductive timing across populations in two songbird species

    Climate change has led to changes in the strength of directional selection on seasonal timing. Understanding the causes and consequences of these changes is crucial to predict the impact of climate change. But are observed patterns in one population generalizable to others, and can spatial variation in selection be explained by environmental variation among populations? We used long-term data (1955–2022) on blue and great tits co-occurring in four locations across the Netherlands to assess inter-population variation in temporal patterns of selection on laying date. To analyse selection, we combine reproduction and adult survival into a joined fitness measure. We found distinct spatial variation in temporal patterns of selection which overall acted towards earlier laying, and which was due to selection through reproduction rather than through survival. The underlying relationships between temperature, bird and caterpillar phenology were however the same across populations, and the spatial variation in selection patterns is thus caused by spatial variation in the temperatures and other habitat characteristics to which birds and caterpillars respond. This underlines that climate change is not necessarily equally affecting populations, but that we can understand this spatial variation, which enables us to predict climate change effects on selection for other populations.
    https://doi.org/10.1098/rspb.2023.1474
  • Evolution Letters
    12-10-2023

    The genomics of adaptation to climate in European great tit (Parus major) populations

    Joanne C. Stonehouse, Lewis G. Spurgin, Veronika Laine, Mirte Bosse, Martien A.M. Groenen, Kees van Oers, Ben C. Sheldon, Marcel E. Visser, Jon Slate
    The recognition that climate change is occurring at an unprecedented rate means that there is increased urgency in understanding how organisms can adapt to a changing environment. Wild great tit (Parus major) populations represent an attractive ecological model system to understand the genomics of climate adaptation. They are widely distributed across Eurasia and they have been documented to respond to climate change. We performed a Bayesian genome-environment analysis, by combining local climate data with single nucleotide polymorphisms genotype data from 20 European populations (broadly spanning the species’ continental range). We found 36 genes putatively linked to adaptation to climate. Following an enrichment analysis of biological process Gene Ontology (GO) terms, we identified over-represented terms and pathways among the candidate genes. Because many different genes and GO terms are associated with climate variables, it seems likely that climate adaptation is polygenic and genetically complex. Our findings also suggest that geographical climate adaptation has been occurring since great tits left their Southern European refugia at the end of the last ice age. Finally, we show that substantial climate-associated genetic variation remains, which will be essential for adaptation to future changes.
    https://doi.org/10.1093/evlett/qrad043
  • Ethology
    09-2023

    Female great tits (Parus major) reproduce earlier when paired with a male they prefer

    Ségolène Delaitre, Kees van Oers, Marcel E. Visser, Samuel P. Caro

    Mate choice is a key component of reproductive biology. Females often prefer certain males but do females modulate their reproductive investment depending on whether they are mated with their preferred partner? We investigated this question in great tits (Parus major) where we subjected 36 females to a six-choice mate preference test. Male morphological traits and the female's own characteristics did not influence the preference females expressed. We however found that females spent more time near more exploratory males. We then paired females with one of the males in indoor aviaries, and subsequently monitored their reproductive investment (through measurement of plasma 17β-oestradiol concentrations, first egg date, clutch size and egg size). Females that were mated with a male for which they had a strong preference laid their first clutch significantly earlier in the season than females paired with a male they less preferred. Our results show that mate preference influences reproductive investment in great tits, thereby linking mate choice to bird reproductive decisions.

    https://doi.org/10.1111/eth.13381
  • Proceedings of the Royal Society B: Biological Sciences
    30-08-2023

    Phenological mismatch affects individual fitness and population growth in the winter moth

    Natalie van Dis, Geert-Jan Sieperda, Vidisha Bansal, Bart van Lith, Bregje Wertheim, Marcel E. Visser

    Climate change can severely impact species that depend on temporary resources by inducing phenological mismatches between consumer and resource seasonal timing. In the winter moth, warmer winters caused eggs to hatch before their food source, young oak leaves, became available. This phenological mismatch changed the selection on the temperature sensitivity of egg development rate. However, we know little about the fine-scale fitness consequences of phenological mismatch at the individual level and how this mismatch affects population dynamics in the winter moth. To determine the fitness consequences of mistimed egg hatching relative to timing of oak budburst, we quantified survival and pupation weight in a feeding experiment. We found that mismatch greatly increased mortality rates of freshly hatched caterpillars, as well as affecting caterpillar growth and development time. We then investigated whether these individual fitness consequences have population-level impacts by estimating the effect of phenological mismatch on population dynamics, using our long-term data (1994-2021) on relative winter moth population densities at four locations in The Netherlands. We found a significant effect of mismatch on population density with higher population growth rates in years with a smaller phenological mismatch. Our results indicate that climate change-induced phenological mismatch can incur severe individual fitness consequences that can impact population density in the wild.

    https://doi.org/10.1098/rspb.2023.0414
  • Nature Climate Change
    14-08-2023

    Detecting climate signals cascading through levels of biological organization

    Marlène Gamelon, Stéphanie Jenouvrier, Melanie Lindner, Bernt-Erik Sæther, Marcel E. Visser
    Threats to species under climate change can be understood as a time at which the signal of climate change in ecological processes emerges from the noise of ecosystem variability, defined as ‘time of emergence’ (ToE). Here we show that ToE for the great tit (Parus major) will occur earlier at the level of population size than trait (laying date) and vital rates (survival, recruitment) under the RCP 8.5 scenario, suggesting an amplified climate change signal at the population level. ToE thus varies across levels of biological organization that filter trends and variability in climate differently. This has implications for the detection of climate impacts on wild species, as a shift in population size may precede changes in traits and vital rates. Further work would need to identify the ecological level that may experience an earlier detection of the climate signal for species with contrasting life histories, climate trends and variability.
    https://doi.org/10.1038/s41558-023-01760-y
  • Proceedings of the Royal Society B: Biological Sciences
    05-07-2023

    Individual life histories

    Joanie Van de Walle, Rémi Fay, Jean Michel Gaillard, Fanie Pelletier, Sandra Hamel, Marlène Gamelon, Christophe Barbraud, F. Guillaume Blanchet, Daniel T. Blumstein, Anne Charmantier, Karine Delord, Benjamin Larue, Julien Martin, James A Mills, Emmanuel Milot, Francine M. Mayer, Jay J. Rotella, Bernt-Erik Sæther, Céline Teplitsky, Martijn van de Pol, Dirk H. Van Vuren, Marcel E. Visser, Caitlin P. Wells, John Yarrall, Stéphanie Jenouvrier
    The slow–fast continuum is a commonly used framework to describe variation in life-history strategies across species. Individual life histories have also been assumed to follow a similar pattern, especially in the pace-of-life syndrome literature. However, whether a slow–fast continuum commonly explains life-history variation among individuals within a population remains unclear. Here, we formally tested for the presence of a slow–fast continuum of life histories both within populations and across species using detailed long-term individual-based demographic data for 17 bird and mammal species with markedly different life histories. We estimated adult lifespan, age at first reproduction, annual breeding frequency, and annual fecundity, and identified the main axes of life-history variation using principal component analyses. Across species, we retrieved the slow–fast continuum as the main axis of life-history variation. However, within populations, the patterns of individual life-history variation did not align with a slow–fast continuum in any species. Thus, a continuum ranking individuals from slow to fast living is unlikely to shape individual differences in life histories within populations. Rather, individual life-history variation is likely idiosyncratic across species, potentially because of processes such as stochasticity, density dependence, and individual differences in resource acquisition that affect species differently and generate non-generalizable patterns across species.
    https://doi.org/10.1098/rspb.2023.0511
  • Science advances
    09-06-2023

    Genotypes selected for early and late avian lay date differ in their phenotype, but not fitness, in the wild

    Melanie Lindner, Jip Ramakers, Irene C. Verhagen, Barbara Tomotani, A.C. Mateman, Phillip Gienapp, Marcel E. Visser
    Global warming has shifted phenological traits in many species, but whether species are able to track further increasing temperatures depends on the fitness consequences of additional shifts in phenological traits. To test this, we measured phenology and fitness of great tits (Parus major) with genotypes for extremely early and late egg lay dates, obtained from a genomic selection experiment. Females with early genotypes advanced lay dates relative to females with late genotypes, but not relative to nonselected females. Females with early and late genotypes did not differ in the number of fledglings produced, in line with the weak effect of lay date on the number of fledglings produced by nonselected females in the years of the experiment. Our study is the first application of genomic selection in the wild and led to an asymmetric phenotypic response that indicates the presence of constraints toward early, but not late, lay dates.
    https://doi.org/10.1126/sciadv.ade6350
  • Proceedings of the National Academy of Sciences of the United States of America
    01-05-2023

    The effect of climate change on avian offspring production: A global meta-analysis

    Lucyna Halupka, Debora Arlt, Jere Tolvanen, Alexandre Millon, Pierre Bize, Peter Adamík, Pascal Albert, Wayne J. Arendt, Alexander V. Artemyev, Vittorio Baglione, Jerzy Bańbura, Mirosława Bańbura, Emilio Barba, Robert T. Barrett, Peter H Becker, Eugen Belskii, Mark Bolton, E. Keith Bowers, Joël Bried, Lyanne Brouwer, Monika Bukacińska, Dariusz Bukaciński, Lesley Bulluck, Kate F. Carstens, Inês Catry, Motti Charter, Anna Chernomorets, Rita Covas, Monika Czuchra, Donald C. Dearborn, Florentino de Lope, Adrián S. Di Giacomo, Valery C. Dombrovski, Hugh Drummond, Michael J. Dunn, Tapio Eeva, Louise M. Emmerson, Yngve Espmark, Juan A. Fargallo, Sergey I. Gashkov, Elena Yu. Golubova, Michael Griesser, Michael P. Harris, Jeffrey P. Hoover, Zuzanna Jagiełło, Patrik Karell, Janusz Kloskowski, Walter D. Koenig, Heikki Kolunen, Małgorzata Korczak-Abshire, Erkki Korpimäki, Indrikis Krams, Miloš Krist, Sonja C. Krüger, Boris D. Kuranov, Xavier Lambin, Michael P. Lombardo, Andrey Lyakhov, Alfonso Marzal, Anders P. Møller, Verónica C. Neves, Jan Tøttrup Nielsen, Alexander Numerov, Beata Orłowska, Daniel Oro, Markus Öst, Richard A. Phillips, Hannu Pietiäinen, Vicente Polo, Jiří Porkert, Jaime Potti, Hannu Pöysä, Thierry Printemps, Jouke Prop, Petra Quillfeldt, Jaime Albino Ramos, Pierre-Alain Ravussin, Robert N. Rosenfield, Alexandre Roulin, Dustin R. Rubenstein, Irina E. Samusenko, Denis A. Saunders, Michael Schaub, Juan Carlos Senar, Fabrizio Sergio, Tapio Solonen, Diana V Solovyeva, Janusz Stępniewski, Paul M Thompson, Marcin Tobolka, János Török, Martijn van de Pol, Louis Vernooij, Marcel E. Visser, David F Westneat, Nathaniel T. Wheelwright, Jarosław Wiącek, Karen L. Wiebe, Andrew G. Wood, Andrzej Wuczyński, Dariusz Wysocki, Markéta Zárybnická, Antoni Margalida, Konrad Halupka
    Significance
    Numerous studies have shown that climate change has altered avian timing of breeding. However, little is known about climate-driven changes in offspring production. We collected long-term breeding data on 201 populations of 104 bird species (N = 745,962 clutches) from all continents, between 1970 and 2019, to assess temporal changes in annual offspring production by female breeders in relation to changes in local temperatures and species’ life history traits. Overall, offspring production declined over time, but responses of different populations to rising temperatures were diverse. Our analyses suggest that negative effects of rising temperatures on offspring production will mainly affect migratory and larger-bodied species, whereas smaller-bodied sedentary species may benefit from warmer climate.

    Abstract
    Climate change affects timing of reproduction in many bird species, but few studies have investigated its influence on annual reproductive output. Here, we assess changes in the annual production of young by female breeders in 201 populations of 104 bird species (N = 745,962 clutches) covering all continents between 1970 and 2019. Overall, average offspring production has declined in recent decades, but considerable differences were found among species and populations. A total of 56.7% of populations showed a declining trend in offspring production (significant in 17.4%), whereas 43.3% exhibited an increase (significant in 10.4%). The results show that climatic changes affect offspring production through compounded effects on ecological and life history traits of species. Migratory and larger-bodied species experienced reduced offspring production with increasing temperatures during the chick-rearing period, whereas smaller-bodied, sedentary species tended to produce more offspring. Likewise, multi-brooded species showed increased breeding success with increasing temperatures, whereas rising temperatures were unrelated to reproductive success in single-brooded species. Our study suggests that rapid declines in size of bird populations reported by many studies from different parts of the world are driven only to a small degree by changes in the production of young.
    https://doi.org/10.1073/pnas.2208389120
  • Movement Ecology
    26-04-2023

    Combining acoustic tracking and LiDAR to study bat flight behaviour in three-dimensional space

    Claire Hermans, Jens koblitz, Harm Bartholomeus, Peter Stilz, Marcel E. Visser, Kamiel Spoelstra
    Background: Habitat structure strongly influences niche differentiation, facilitates predator avoidance, and drives
    species-specific foraging strategies of bats. Vegetation structure is also a strong driver of echolocation call character-
    istics. The fine-scale assessment of how bats utilise such structures in their natural habitat is instrumental in under-
    standing how habitat composition shapes flight- and acoustic behaviour. However, it is notoriously difficult to study
    their species-habitat relationship in situ.
    Methods: Here, we describe a methodology combining Light Detection and Ranging (LiDAR) to characterise three-
    dimensional vegetation structure and acoustic tracking to map bat behaviour. This makes it possible to study fine-
    scale use of habitat by bats, which is essential to understand spatial niche segregation in bats. Bats were acoustically
    tracked with microphone arrays and bat calls were classified to bat guild using automated identification. We did this
    in multiple LiDAR scanned vegetation plots in forest edge habitat. The datasets were spatially aligned to calculate the
    distance between bats’ positions and vegetation structures.
    Results: Our results are a proof of concept of combining LiDAR with acoustic tracking. Although it entails challenges
    with combining mass-volumes of fine-scale bat movements and vegetation information, we show the feasibility and
    potential of combining those two methods through two case studies. The first one shows stereotyped flight patterns
    of pipistrelles around tree trunks, while the second one presents the distance that bats keep to the vegetation in the
    presence of artificial light.
    Conclusion: By combining bat guild specific spatial behaviour with precise information on vegetation structure, the
    bat guild specific response to habitat characteristics can be studied in great detail. This opens up the possibility to
    address yet unanswered questions on bat behaviour, such as niche segregation or response to abiotic factors in inter-
    action with natural vegetation. This combination of techniques can also pave the way for other applications linking
    movement patterns of other vocalizing animals and 3D space reconstruction.
    https://doi.org/10.1186/s40462-023-00387-0
  • American Naturalist
    03-02-2023

    Estimating Density Dependence, Environmental Variance, and Long-Term Selection on a Stage-Structured Life History

    R. Lande, V. Grøtan, S. Engen, Marcel E. Visser, Bernt-Erik Sæther
    A method for analyzing long-term demographic data on density-dependent stage-structured populations in a stochastic environment is derived to facilitate comparison of populations and species with different life histories. We assume that a weighted sum of stage abundances, N, exerts density dependence on stage-specific vital rates of survival and reproduction and that N has a small or moderate coefficient of variation. The dynamics of N are approximated as a univariate stochastic process governed by three key parameters: the density-independent growth rate, the net density dependence, and environmental variance in the life history. We show how to estimate the relative weighs of stages in N and the key parameters. Life history evolution represents a stochastic maximization of a simple function of the key parameters. The long-term selection gradient on the life history can be expressed as a vector of sensitivities of this function with respect to density-independent, density-dependent, and stochastic components of the vital rates. To illustrate the method, we analyze 38 years of demographic data on a great tit population, estimating the key parameters, which accurately predict the observed mean, coefficient of variation, and fluctuation rate of N; we also evaluate the long-term selection gradient on the life history.
    https://doi.org/10.1086/723211
  • Ecology
    21-12-2022

    Temperature synchronizes temporal variation in laying dates across European hole‐nesting passerines

    Stefan Vriend, Vidar Grøtan, Marlène Gamelon, Frank Adriaensen, Markus P. Ahola, Elena Álvarez, Liam Bailey, Emilio Barba, Jean-Charles Bouvier, Malcolm D. Burgess, Andrey Bushuev, Carlos Camacho, David Canal, Anne Charmantier, Ella F. Cole, Camillo A. Cusimano, Blandine F. Doligez, Szymon M. Drobniak, Anna Dubiec, Marcel Eens, Tapio Eeva, Kjell Einar Erikstad, Peter N. Ferns, Anne E. Goodenough, Ian R. Hartley, Shelley A. Hinsley, Elena V. Ivankina, Rimvydas Juškaitis, Bart Kempenaers, Anvar B. Kerimov, John Atle Kålås, Claire Lavigne, Agu Leivits, Mark C. Mainwaring, Jesús Martínez-Padilla, Erik Matthysen, Kees van Oers, Markku Orell, Rianne Pinxten, Tone Kristin Reiertsen, Seppo Rytkönen, Juan Carlos Senar, Ben C. Sheldon, Alberto Sorace, János Török, Emma Vatka, Marcel E. Visser, Bernt-Erik Sæther
    Identifying the environmental drivers of variation in fitness-related traits is a central objective in ecology and evolutionary biology. Temporal fluctuations of these environmental drivers are often synchronized at large spatial scales. Yet, whether synchronous environmental conditions can generate spatial synchrony in fitness-related trait values (i.e., correlated temporal trait fluctuations across populations) is poorly understood. Using data from long-term monitored populations of blue tits (Cyanistes caeruleus, n = 31), great tits (Parus major, n = 35), and pied flycatchers (Ficedula hypoleuca, n = 20) across Europe, we assessed the influence of two local climatic variables (mean temperature and mean precipitation in February–May) on spatial synchrony in three fitness-related traits: laying date, clutch size, and fledgling number. We found a high degree of spatial synchrony in laying date but a lower degree in clutch size and fledgling number for each species. Temperature strongly influenced spatial synchrony in laying date for resident blue tits and great tits but not for migratory pied flycatchers. This is a relevant finding in the context of environmental impacts on populations because spatial synchrony in fitness-related trait values among populations may influence fluctuations in vital rates or population abundances. If environmentally induced spatial synchrony in fitness-related traits increases the spatial synchrony in vital rates or population abundances, this will ultimately increase the risk of extinction for populations and species. Assessing how environmental conditions influence spatiotemporal variation in trait values improves our mechanistic understanding of environmental impacts on populations.
    https://doi.org/10.1002/ecy.3908
  • Current Biology
    05-12-2022

    Species-specific song responses emerge as a by-product of tuning to the local dialect

    David Wheatcroft, Louis Bliard, Myriam El Harouchi, David López-Idiáquez, Tiia Kärkkäinen, Fanny Linn H. Kraft, Jaime Muriel, Samyuktha Rajan, Tomas Tuvillo, Malcolm D. Burgess, Alejandro Cantarero, Toni Laaksonen, Jesús Martínez-Padilla, Marcel E. Visser, Anna Qvarnström

    Oscine birds preferentially respond to certain sounds over others from an early age, which focuses subsequent learning onto sexually relevant songs.1,2,3 Songs vary both across species and, due to cultural evolution, among populations of the same species. As a result, early song responses are expected to be shaped by selection both to avoid the fitness costs of cross-species learning4 and to promote learning of population-typical songs.5 These sources of selection are not mutually exclusive but can result in distinct geographic patterns of song responses in juvenile birds: if the risks of interspecific mating are the main driver of early song discrimination, then discrimination should be strongest where closely related species co-occur.4 In contrast, if early discrimination primarily facilitates learning local songs, then it should be tuned to songs typical of the local dialect.5,6,7 Here, we experimentally assess the drivers of song discrimination in nestling pied flycatchers (Ficedula hypoleuca). We first demonstrate that early discrimination against the songs of the closely related collared flycatcher (F. albicollis) is not strongly affected by co-occurrence. Second, across six European populations, we show that nestlings’ early song responses are tuned to their local song dialect and that responses to the songs of collared flycatchers are similarly weak as to those of other conspecific dialects. Taken together, these findings provide clear experimental support for the hypothesis that cultural evolution, in conjunction with associated learning predispositions, drives the emergence of pre-mating reproductive barriers.

    https://doi.org/10.1016/j.cub.2022.09.063
  • Molecular Ecology
    11-2022

    Transcriptional regulation underlying the temperature response of embryonic development rate in the winter moth

    Natalie van Dis, Judith Risse, Agata Pijl, Roelof A Hut, Marcel E. Visser, Bregje Wertheim

    Climate change will strongly affect the developmental timing of insects, as their development rate depends largely on ambient temperature. However, we know little about the genetic mechanisms underlying the temperature sensitivity of embryonic development in insects. We investigated embryonic development rate in the winter moth (Operophtera brumata), a species with egg dormancy which has been under selection due to climate change. We used RNA sequencing to investigate which genes are involved in the regulation of winter moth embryonic development rate in response to temperature. Over the course of development, we sampled eggs before and after an experimental change in ambient temperature, including two early development weeks when the temperature sensitivity of eggs is low and two late development weeks when temperature sensitivity is high. We found temperature-responsive genes that responded in a similar way across development, as well as genes with a temperature response specific to a particular development week. Moreover, we identified genes whose temperature effect size changed around the switch in temperature sensitivity of development rate. Interesting candidate genes for regulating the temperature sensitivity of egg development rate included genes involved in histone modification, hormonal signalling, nervous system development and circadian clock genes. The diverse sets of temperature-responsive genes we found here indicate that there are many potential targets of selection to change the temperature sensitivity of embryonic development rate. Identifying for which of these genes there is genetic variation in wild insect populations will give insight into their adaptive potential in the face of climate change.

    https://doi.org/10.1111/mec.16705
  • Journal of Animal Ecology
    11-01-2022

    The opportunity for selection

    Thomas Reed, Marcel E. Visser, Robin S. Waples

    Natural selection can only occur if individuals differ in fitness. For this reason, the variance in relative fitness has been equated with the ‘opportunity for selection’ ((Formula presented.)), which has a long, albeit somewhat controversial, history. In this paper we discuss the use/misuse of (Formula presented.) and related metrics in evolutionary ecology. The opportunity is only realised if some fraction of (Formula presented.) is caused by trait variation. Thus, (Formula presented.) does not imply that selection is occurring, as sometimes erroneously assumed, because all fitness variation could be independent of phenotype. The selection intensity on any given trait cannot exceed (Formula presented.), but this upper limit will never be reached because (a) stochastic factors always affect fitness, and (b) there might be multiple traits under selection. The expected magnitude of the stochastic component of (Formula presented.) is negatively correlated with mean fitness. Uncertainty in realised (Formula presented.) is also larger when mean fitness or population/sample size are low. Variation in (Formula presented.) across time or space thus can be dominated (or solely driven) by variation in the strength of demographic stochasticity. We illustrate these points using simulations and empirical data from a population study on great tits Parus major. Our analysis shows that the scope for fecundity selection in the great tits is substantially higher when using annual number of recruits as the fitness measure, rather than fledglings or eggs, even after adjusting for the dependence of (Formula presented.) on mean fitness. This suggests nonrandom survival of juveniles across families between life stages. Indeed, previous work on this population has shown that offspring recruitment is often nonrandom with respect to clutch size and laying date of parents, for example. We conclude that one cannot make direct inferences about selection based on fitness data alone. However, examining variation in (Formula presented.) (the opportunity for fecundity selection adjusted for mean fitness) across life stages, years or environments can offer clues as to when/where fecundity selection might be strongest, which can be useful for research planning and experimental design.

    https://doi.org/10.1111/1365-2656.13841
  • Scientific Reports
    2022

    Integrated molecular and behavioural data reveal deep circadian disruption in response to artificial light at night in male Great tits (Parus major)

    Davide Dominoni, Maaike de Jong, Kees van Oers, Peter O’Shaughnessy, Gavin J. Blackburn, Els Atema, A.C. Mateman, Pietro B. D’Amelio, Lisa Trost, Michelle Bellingham, Jessica Clark, Marcel E. Visser, Barbara Helm

    Globally increasing levels of artificial light at night (ALAN) are associated with shifting rhythms of behaviour in many wild species. However, it is unclear whether changes in behavioural timing are paralleled by consistent shifts in the molecular clock and its associated physiological pathways. Inconsistent shifts between behavioural and molecular rhythms, and between different tissues and physiological systems, disrupt the circadian system, which coordinates all major body functions. We therefore compared behavioural, transcriptional and metabolomic responses of captive great tits (Parus major) to three ALAN intensities or to dark nights, recording activity and sampling brain, liver, spleen and blood at mid-day and midnight. ALAN advanced wake-up time, and this shift was paralleled by advanced expression of the clock gene BMAL1 in all tissues, suggesting close links between behaviour and clock gene expression across tissues. However, further analysis of gene expression and metabolites revealed that clock shifts were inconsistent across physiological systems. Untargeted metabolomic profiling showed that only 9.7% of the 755 analysed metabolites followed the behavioural shift. This high level of desynchronization indicates that ALAN disrupted the circadian system on a deep, easily overlooked level. Thus, circadian disruption could be a key mediator of health impacts of ALAN on wild animals.

    https://doi.org/10.1038/s41598-022-05059-4
  • Molecular Ecology Resources
    2022

    Performance of methods to detect genetic variants from bisulphite sequencing data in a non-model species

    Melanie Lindner, F. Gawehns, Sebastiaan te Molder, Marcel E. Visser, Kees van Oers, Veronika Laine

    The profiling of epigenetic marks like DNA methylation has become a central aspect of studies in evolution and ecology. Bisulphite sequencing is commonly used for assessing genome-wide DNA methylation at single nucleotide resolution but these data can also provide information on genetic variants like single nucleotide polymorphisms (SNPs). However, bisulphite conversion causes unmethylated cytosines to appear as thymines, complicating the alignment and subsequent SNP calling. Several tools have been developed to overcome this challenge, but there is no independent evaluation of such tools for non-model species, which often lack genomic references. Here, we used whole-genome bisulphite sequencing (WGBS) data from four female great tits (Parus major) to evaluate the performance of seven tools for SNP calling from bisulphite sequencing data. We used SNPs from whole-genome resequencing data of the same samples as baseline SNPs to assess common performance metrics like sensitivity, precision, and the number of true positive, false positive, and false negative SNPs for the full range of variant and genotype quality values. We found clear differences between the tools in either optimizing precision (Bis-SNP), sensitivity (biscuit), or a compromise between both (all other tools). Overall, the choice of SNP caller strongly depends on which performance parameter should be maximized and whether ascertainment bias should be minimized to optimize downstream analysis, highlighting the need for studies that assess such differences.

    https://doi.org/10.1111/1755-0998.13493
  • Evolution
    2022

    Population bottleneck has only marginal effect on fitness evolution and its repeatability in dioecious Caenorhabditis elegans

    Karen Bisschop, Thomas Blankers, Janine Mariën, Meike T. Wortel, Martijn Egas, Astrid T. Groot, Marcel E. Visser, Jacintha Ellers

    The predictability of evolution is expected to depend on the relative contribution of deterministic and stochastic processes. This ratio is modulated by effective population size. Smaller effective populations harbor less genetic diversity and stochastic processes are generally expected to play a larger role, leading to less repeatable evolutionary trajectories. Empirical insight into the relationship between effective population size and repeatability is limited and focused mostly on asexual organisms. Here, we tested whether fitness evolution was less repeatable after a population bottleneck in obligately outcrossing populations of Caenorhabditis elegans. Replicated populations founded by 500, 50, or five individuals (no/moderate/strong bottleneck) were exposed to a novel environment with a different bacterial prey. As a proxy for fitness, population size was measured after one week of growth before and after 15 weeks of evolution. Surprisingly, we found no significant differences among treatments in their fitness evolution. Even though the strong bottleneck reduced the relative contribution of selection to fitness variation, this did not translate to a significant reduction in the repeatability of fitness evolution. Thus, although a bottleneck reduced the contribution of deterministic processes, we conclude that the predictability of evolution may not universally depend on effective population size, especially in sexual organisms.

    https://doi.org/10.1111/evo.14556
  • Nature Communications
    2022

    Bird populations most exposed to climate change are less sensitive to climatic variation

    Liam Bailey, Martijn van de Pol, Frank Adriaensen, Aneta Arct, Emilio Barba, Paul E. Bellamy, Suzanne Bonamour, Jean-Charles Bouvier, Malcolm D. Burgess, Anne Charmantier, Camillo A. Cusimano, Blandine F. Doligez, Szymon M. Drobniak, Anna Dubiec, Marcel Eens, Tapio Eeva, Peter N. Ferns, Anne E. Goodenough, Ian R. Hartley, Shelley A. Hinsley, Elena V. Ivankina, Rimvydas Juškaitis, Bart Kempenaers, Anvar B. Kerimov, Claire Lavigne, Agu Leivits, Mark C. Mainwaring, Erik Matthysen, Jan-Åke Nilsson, Markku Orell, Seppo Rytkönen, Juan Carlos Senar, Ben C. Sheldon, Alberto Sorace, Martyn J. Stenning, János Török, Kees van Oers, Emma Vatka, Stefan Vriend, Marcel E. Visser

    The phenology of many species shows strong sensitivity to climate change; however, with few large scale intra-specific studies it is unclear how such sensitivity varies over a species’ range. We document large intra-specific variation in phenological sensitivity to temperature using laying date information from 67 populations of two co-familial European songbirds, the great tit (Parus major) and blue tit (Cyanistes caeruleus), covering a large part of their breeding range. Populations inhabiting deciduous habitats showed stronger phenological sensitivity than those in evergreen and mixed habitats. However, populations with higher sensitivity tended to have experienced less rapid change in climate over the past decades, such that populations with high phenological sensitivity will not necessarily exhibit the strongest phenological advancement. Our results show that to effectively assess the impact of climate change on phenology across a species’ range it will be necessary to account for intra-specific variation in phenological sensitivity, climate change exposure, and the ecological characteristics of a population.

    https://doi.org/10.1038/s41467-022-29635-4
  • Ecology Letters
    2022

    Temporal correlations among demographic parameters are ubiquitous but highly variable across species

    Rémi Fay, Sandra Hamel, Martijn van de Pol, Jean Michel Gaillard, Nigel G. Yoccoz, Paul Acker, Matthieu Authier, Benjamin Larue, Christie Le Coeur, Kaitlin R. Macdonald, Alex Nicol-Harper, Christophe Barbraud, Christophe Bonenfant, Dirk H. Van Vuren, Emmanuelle Cam, Karine Delord, Marlène Gamelon, Maria Moiron, Fanie Pelletier, Jay J. Rotella, Céline Teplitsky, Marcel E. Visser, Caitlin P. Wells, Nathaniel T. Wheelwright, Stéphanie Jenouvrier, Bernt-Erik Sæther
    Temporal correlations among demographic parameters can strongly influence population dynamics. Our empirical knowledge, however, is very limited regarding the direction and the magnitude of these correlations and how they vary among demographic parameters and species? life histories. Here, we use long-term demographic data from 15 bird and mammal species with contrasting pace of life to quantify correlation patterns among five key demographic parameters: juvenile and adult survival, reproductive probability, reproductive success and productivity. Correlations among demographic parameters were ubiquitous, more frequently positive than negative, but strongly differed across species. Correlations did not markedly change along the slow-fast continuum of life histories, suggesting that they were more strongly driven by ecological than evolutionary factors. As positive temporal demographic correlations decrease the mean of the long-run population growth rate, the common practice of ignoring temporal correlations in population models could lead to the underestimation of extinction risks in most species.
    https://doi.org/10.1111/ele.14026
  • Trends in Ecology and Evolution
    2022

    Biological Earth observation with animal sensors

    Walter Jetz, Grigori Tertitski, Roland W. Kays, Uschi Mueller, Martin Wikelski, Susanne Åkesson, Yuriy A. Anisimov, Aleksey Antonov, Walter Arnold, Franz Bairlein, Oriol Baltà, Diane Baum, Mario Beck, Olga Belonovich, Mikhail Belyaev, Matthias Berger, Peter Berthold, Steffen Bittner, Stephen Blake, Barbara Block, Daniel Bloche, Katrin Boehning-Gaese, Gil Bohrer, Julia Bojarinova, Gerhard Bommas, Oleg Bourski, Albert Bragin, Alexandr Bragin, Rachel Bristol, Vojtěch Brlík, Victor N Bulyuk, Francesca Cagnacci, Ben Carlson, Taylor K. Chapple, Kalkidan F. Chefira, Yachang Cheng, Nikita Chernetsov, Grzegorz Cierlik, Simon S. Christiansen, Oriol Clarabuch, William Cochran, Jamie Margaret Cornelius, Iain Couzin, Margret C. Crofoot, Andrea Kölzsch, Morrison Pot, Froukje Rienks, Kamiel Spoelstra, Henk P. van der Jeugd, Marcel E. Visser

    Space-based tracking technology using low-cost miniature tags is now delivering data on fine-scale animal movement at near-global scale. Linked with remotely sensed environmental data, this offers a biological lens on habitat integrity and connectivity for conservation and human health; a global network of animal sentinels of environmental change.

    https://doi.org/10.1016/j.tree.2021.11.011
  • Science
    2022

    Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals

    Timothée Bonnet, Michael B. Morrissey, Pierre de Villemereuil, Susan C. Alberts, Peter Arcese, Liam Bailey, Stan Boutin, Patricia Brekke, Lauren J.N. Brent, Glauco Camenisch, Anne Charmantier, Tim H. Clutton-Brock, Andrew Cockburn, David W. Coltman, Alexandre Courtiol, Eve Davidian, Simon R. Evans, John G. Ewen, Marco Festa-Bianchet, Christophe de Franceschi, Lars Gustafsson, Oliver P. Höner, Thomas M. Houslay, Lukas F. Keller, Marta Manser, Andrew G. McAdam, Emily McLean, Pirmin Nietlisbach, Helen L. Osmond, Josephine M. Pemberton, Erik Postma, Jane M. Reid, Alexis Rutschmann, Anna W. Santure, Ben C. Sheldon, Jon Slate, Céline Teplitsky, Marcel E. Visser, Bettina Wachter, Loeske E. B. Kruuk

    The rate of adaptive evolution, the contribution of selection to genetic changes that increase mean fitness, is determined by the additive genetic variance in individual relative fitness. To date, there are few robust estimates of this parameter for natural populations, and it is therefore unclear whether adaptive evolution can play a meaningful role in short-term population dynamics. We developed and applied quantitative genetic methods to long-term datasets from 19 wild bird and mammal populations and found that, while estimates vary between populations, additive genetic variance in relative fitness is often substantial and, on average, twice that of previous estimates. We show that these rates of contemporary adaptive evolution can affect population dynamics and hence that natural selection has the potential to partly mitigate effects of current environmental change.

    https://doi.org/10.1126/science.abk0853
  • Frontiers in Ecology and Evolution
    08-12-2021

    11 Pressing Research Questions on How Light Pollution Affects Biodiversity

    Franz Hölker, Janine Bolliger, Thomas W. Davies, Simone Giavi, Andreas Jechow, Gregor Kalinkat, Travis Longcore, Kamiel Spoelstra, Svenja Tidau, Marcel E. Visser, Eva Knop

    Artificial light at night (ALAN) is closely associated with modern societies and is rapidly increasing worldwide. A dynamically growing body of literature shows that ALAN poses a serious threat to all levels of biodiversity—from genes to ecosystems. Many “unknowns” remain to be addressed however, before we fully understand the impact of ALAN on biodiversity and can design effective mitigation measures. Here, we distilled the findings of a workshop on the effects of ALAN on biodiversity at the first World Biodiversity Forum in Davos attended by several major research groups in the field from across the globe. We argue that 11 pressing research questions have to be answered to find ways to reduce the impact of ALAN on biodiversity. The questions address fundamental knowledge gaps, ranging from basic challenges on how to standardize light measurements, through the multi-level impacts on biodiversity, to opportunities and challenges for more sustainable use.

    https://doi.org/10.3389/fevo.2021.767177
  • Journal of Applied Ecology
    10-2021

    Urban street lighting differentially affects community attributes of airborne and ground-dwelling invertebrate assemblages

    Martin T. Lockett, Therésa M. Jones, Mark A. Elgar, Kevin J. Gaston, Marcel E. Visser, Gareth R. Hopkins

    The introduction of artificial light at night (ALAN) into natural and urbanised landscapes is a known and highly pervasive disruptor of invertebrate communities. However, the effect of variation in intensity and spectra of ALAN on invertebrate communities inhabiting different spatial niches is little understood. Further, the remarkable ability of ALAN to continue to disrupt biodiversity even in chronically illuminated urban landscapes is not often acknowledged. Here, we simultaneously sampled airborne and ground-dwelling invertebrate assemblages under and between urban street lights to explore the effects on community composition and abundance of (a) proximity to decadal (i.e. long-illuminated) nocturnal street lighting and (b) variation in the spectral output of light. The two assemblages responded differently. For airborne invertebrates, night-time abundance doubled, and night-time assemblage composition was significantly different for traps under, compared with between, street lights. These differences in abundance were not affected by street light intensity, and were absent in day samples, suggesting that even weak ALAN may be causing short-term redistribution of nocturnal invertebrates. Further, the abundance (but not composition) effects of ALAN on airborne invertebrates increased when the street lights emitted a higher proportion of short-wavelength light. In contrast, for ground-dwelling invertebrates, we found only marginal effects of proximity and spectrum of lighting on abundance and no effect on assemblage composition. However, more intense street lighting reduced abundance and altered composition at traps both under and between lights. Synthesis and Applications. Public lighting managers must consider ALAN impacts on invertebrate communities not only when introducing ALAN to naïve environments, but also when changing lighting in areas that are highly urbanised and exposed to decades of ALAN. Further, lighting proposals and environmental monitoring of invertebrate communities must take into account the effects on both ground-dwelling and airborne assemblages, as these may respond very differently to the presence, intensity and spectrum of ALAN.

    https://doi.org/10.1111/1365-2664.13969
  • Journal of Experimental Biology
    01-09-2021

    Timing of increased temperature sensitivity coincides with nervous system development in winter moth embryos

    Natalie van Dis, Maurijn van der Zee, Roelof A Hut, Bregje Wertheim, Marcel E. Visser
    Climate change is rapidly altering the environment and many species will need to genetically adapt their seasonal timing to keep up with these changes. Insect development rate is largely influenced by temperature, but we know little about the mechanisms underlying the temperature sensitivity of development. Here, we investigate seasonal timing of egg hatching in the winter moth, one of the few species which has been found to genetically adapt to climate change, likely through selection on temperature sensitivity of egg development rate. To study when during development winter moth embryos are most sensitive to changes in ambient temperature, we gave eggs an increase or decrease in temperature at different moments during their development. We measured their developmental progression and time of egg hatching, and used fluorescence microscopy to construct a timeline of embryonic development for the winter moth. We found that egg development rate responded more strongly to temperature once embryos were in the fully extended germband stage. This is the phylotypic stage at which all insect embryos have developed a rudimentary nervous system. Furthermore, at this stage, timing of ecdysone signaling determines developmental progression, which could act as an environment dependent gateway. Intriguingly, this may suggest that, from the phylotypic stage onward, insect embryos can start to integrate internal and environmental stimuli to actively regulate important developmental processes. As we found evidence that there is genetic variation for temperature sensitivity of egg development rate in our study population, such regulation could be a target of selection imposed by climate change.
    https://doi.org/10.1242/jeb.242554
  • Frontiers in Ecology and Evolution
    22-02-2021

    Integrating Causal and Evolutionary Analysis of Life-History Evolution

    Barbara Tomotani, Phillip Gienapp, Iván De la Hera, Martijn Terpstra, F. Pulido, Marcel E. Visser

    In migratory species, the timing of arrival at the breeding grounds is a life-history trait with major fitness consequences. The optimal arrival date varies from year-to-year, and animals use cues to adjust their arrival dates to match this annual variation. However, which cues they use to time their arrival and whether these cues actually predict the annual optimal arrival date is largely unknown. Here, we integrate causal and evolutionary analysis by identifying the environmental variables used by a migratory songbird to time its arrival dates and testing whether these environmental variables also predicted the optimal time to arrive. We used 11 years of male arrival data of a pied flycatcher population. Specifically, we tested whether temperature and normalized difference vegetation index (NDVI) values from their breeding grounds in the Netherlands and from their wintering grounds in Ivory Coast explained the variation in arrival date, and whether these variables correlated with the position of the annual fitness peak at the breeding grounds. We found that temperature and NDVI, both from the wintering and the breeding grounds, explained the annual variation in arrival date, but did not correlate with the optimal arrival date. We explore three alternative explanations for this lack of correlation. Firstly, the date of the fitness peak may have been incorrectly estimated because a potentially important component of fitness (i.e., migration date dependent mortality en route or directly upon arrival) could not be measured. Secondly, we focused on male timing but the fitness landscape is also likely to be shaped by female timing. Finally, the correlation has recently disappeared because climate change disrupted the predictive value of the cues that the birds use to time their migration. In the latter case, birds may adapt by altering their sensitivity to temperature and NDVI.

    https://doi.org/10.3389/fevo.2021.630823
  • Proceedings of the Royal Society B: Biological Sciences
    2021

    Recent natural variability in global warming weakened phenological mismatch and selection on seasonal timing in great tits (Parus major)

    Marcel E. Visser, Melanie Lindner, Phillip Gienapp, Matthew C. Long, Stéphanie Jenouvrier
    Climate change has led to phenological shifts in many species, but with large variation in magnitude among species and trophic levels. The poster child example of the resulting phenological mismatches between the phenology of predators and their prey is the great tit (Parus major), where this mismatch led to directional selection for earlier seasonal breeding. Natural climate variability can obscure the impacts of climate change over certain periods, weakening phenological mismatching and selection. Here, we show that selection on seasonal timing indeed weakened significantly over the past two decades as increases in late spring temperatures have slowed down. Consequently, there has been no further advancement in the date of peak caterpillar food abundance, while great tit phenology has continued to advance, thereby weakening the phenological mismatch. We thus show that the relationships between temperature, phenologies of prey and predator, and selection on predator phenology are robust, also in times of a slowdown of warming. Using projected temperatures from a large ensemble of climate simulations that take natural climate variability into account, we show that prey phenology is again projected to advance faster than great tit phenology in the coming decades, and therefore that long-term global warming will intensify phenological mismatches.
    https://doi.org/10.1098/rspb.2021.1337
  • Nature Communications
    2021

    Continent-wide genomic signatures of adaptation to urbanisation in a songbird across Europe

    Pablo Salmón, Arne Jacobs, Dag Ahrén, Clotilde Biard, N.J. Dingemanse, Davide Dominoni, Barbara Helm, Max Lundberg, Juan Carlos Senar, Philipp Sprau, Marcel E. Visser, Caroline Isaksson

    Urbanisation is increasing worldwide, and there is now ample evidence of phenotypic changes in wild organisms in response to this novel environment. Yet, the genetic changes and genomic architecture underlying these adaptations are poorly understood. Here, we genotype 192 great tits (Parus major) from nine European cities, each paired with an adjacent rural site, to address this major knowledge gap in our understanding of wildlife urban adaptation. We find that a combination of polygenic allele frequency shifts and recurrent selective sweeps are associated with the adaptation of great tits to urban environments. While haplotypes under selection are rarely shared across urban populations, selective sweeps occur within the same genes, mostly linked to neural function and development. Collectively, we show that urban adaptation in a widespread songbird occurs through unique and shared selective sweeps in a core-set of behaviour-linked genes.

    https://doi.org/10.1038/s41467-021-23027-w
  • Molecular Ecology
    2021

    Rapid changes in DNA methylation associated with the initiation of reproduction in a small songbird

    Melanie Lindner, Veronika Laine, Irene C. Verhagen, Heidi M. Viitaniemi, Marcel E. Visser, Kees van Oers, Arild Husby
    Species with a circannual life cycle need to match the timing of their life history events to the environment to maximize fitness. However, our understanding of how circannual traits such as timing of reproduction are regulated on a molecular level remains limited. Recent studies have implicated that epigenetic mechanisms can be an important part in the processes that regulate circannual traits. Here, we explore the role of DNA methylation in mediating reproductive timing in a seasonally breeding bird species, the great tit (Parus major), using genome‐wide DNA methylation data from individual females that were blood sampled repeatedly throughout the breeding season. We demonstrate rapid and directional changes in DNA methylation within the promoter region of several genes, including a key transcription factor (NR5A1) known from earlier studies to be involved in the initiation of timing of reproduction. Interestingly, the observed changes in DNA methylation at NR5A1 identified here are in line with earlier gene expression studies of reproduction in chicken, indicating that the observed shifts in DNA methylation at this gene can have a regulatory role. Our findings provide an important step towards elucidating the genomic mechanism that mediates seasonal timing of a key life history traits and provide support for the idea that epigenetic mechanisms may play an important role in circannual traits.
    https://doi.org/10.1111/mec.15803
  • BMC Genomics
    2021

    Temporal changes in DNA methylation and RNA expression in a small song bird

    Melanie Lindner, Irene C. Verhagen, Heidi M. Viitaniemi, Veronika Laine, Marcel E. Visser, Arild Husby, Kees van Oers

    Background: DNA methylation is likely a key mechanism regulating changes in gene transcription in traits that show temporal fluctuations in response to environmental conditions. To understand the transcriptional role of DNA methylation we need simultaneous within-individual assessment of methylation changes and gene expression changes over time. Within-individual repeated sampling of tissues, which are essential for trait expression is, however, unfeasible (e.g. specific brain regions, liver and ovary for reproductive timing). Here, we explore to what extend between-individual changes in DNA methylation in a tissue accessible for repeated sampling (red blood cells (RBCs)) reflect such patterns in a tissue unavailable for repeated sampling (liver) and how these DNA methylation patterns are associated with gene expression in such inaccessible tissues (hypothalamus, ovary and liver). For this, 18 great tit (Parus major) females were sacrificed at three time points (n = 6 per time point) throughout the pre-laying and egg-laying period and their blood, hypothalamus, ovary and liver were sampled.

    Results: We simultaneously assessed DNA methylation changes (via reduced representation bisulfite sequencing) and changes in gene expression (via RNA-seq and qPCR) over time. In general, we found a positive correlation between changes in CpG site methylation in RBCs and liver across timepoints. For CpG sites in close proximity to the transcription start site, an increase in RBC methylation over time was associated with a decrease in the expression of the associated gene in the ovary. In contrast, no such association with gene expression was found for CpG site methylation within the gene body or the 10 kb up- and downstream regions adjacent to the gene body.

    Conclusion: Temporal changes in DNA methylation are largely tissue-general, indicating that changes in RBC methylation can reflect changes in DNA methylation in other, often less accessible, tissues such as the liver in our case. However, associations between temporal changes in DNA methylation with changes in gene expression are mostly tissue- and genomic location-dependent. The observation that temporal changes in DNA methylation within RBCs can relate to changes in gene expression in less accessible tissues is important for a better understanding of how environmental conditions shape traits that temporally change in expression in wild populations.

    https://doi.org/10.1186/s12864-020-07329-9
  • Journal of Animal Ecology
    2021

    Connecting the data landscape of long-term ecological studies

    Antica Culina, Frank Adriaensen, Liam Bailey, Malcolm D. Burgess, Anne Charmantier, Ella F. Cole, Tapio Eeva, Erik Matthysen, Chloé R. Nater, Ben C. Sheldon, Bernt-Erik Sæther, Stefan Vriend, Zuzana Zajkova, Peter Adamík, Lucy M. Aplin, Elena Angulo, Alexander V. Artemyev, Emilio Barba, Sanja Barišić, Eduardo Belda, Cemal Can Bilgin, Josefa Bleu, Christiaan Both, Sandra Bouwhuis, Claire J. Branston, Juli Broggi, Terry Burke, Andrey Bushuev, Carlos Camacho, Daniela Campobello, David Canal, Alejandro Cantarero, Samuel P. Caro, Maxime Cauchoix, Alexis Chaine, Mariusz Cichoń, Davor Ćiković, Camillo A. Cusimano, Caroline Deimel, André A Dhondt, N.J. Dingemanse, Blandine F. Doligez, Davide Dominoni, Claire Doutrelant, Szymon M. Drobniak, Anna Dubiec, Marcel Eens, Kjell Einar Erikstad, Silvia Espín, Damien R. Farine, Jordi Figuerola, Pınar Kavak Gülbeyaz, Arnaud Grégoire, Ian R. Hartley, Michaela Hau, Gergely Hegyi, Sabine Hille, C.A. Hinde, Benedikt Holtmann, Tatyana Ilyina, Caroline Isaksson, Arne Iserbyt, Elena V. Ivankina, Wojciech Kania, Bart Kempenaers, Anvar B. Kerimov, Jan Komdeur, Peter Korsten, Miroslav Král, Miloš Krist, Marcel M. Lambrechts, Carlos E. Lara, Agu Leivits, András Liker, Jaanis Lodjak, Marko Mägi, Mark C. Mainwaring, Raivo Mänd, Bruno Massa, Sylvie Massemin, Jesús Martínez-Padilla, Tomasz D. Mazgajski, Adèle Mennerat, Juan Moreno, Alexia Mouchet, Shinichi Nakagawa, Jan-Åke Nilsson, Johan F. Nilsson, Ana C. Norte, Kees van Oers, Markku Orell, Jaime Potti, John L. Quinn, Denis Réale, Tone Kristin Reiertsen, Balázs Rosivall, Andrew F. Russell, Seppo Rytkönen, Pablo Sánchez-Virosta, Eduardo S.A. Santos, Julia Schroeder, Juan Carlos Senar, Gábor Seress, Tore Slagsvold, Marta Szulkin, Céline Teplitsky, Vallo Tilgar, Andrey Tolstoguzov, János Török, Mihai Valcu, Emma Vatka, Simon Verhulst, Hannah Watson, Teru Yuta, José M. Zamora-Marín, Marcel E. Visser
    The integration and synthesis of the data in different areas of science is drastically slowed and hindered by a lack of standards and networking programmes. Long‐term studies of individually marked animals are not an exception. These studies are especially important as instrumental for understanding evolutionary and ecological processes in the wild. Furthermore, their number and global distribution provides a unique opportunity to assess the generality of patterns and to address broad‐scale global issues (e.g. climate change).
    To solve data integration issues and enable a new scale of ecological and evolutionary research based on long‐term studies of birds, we have created the SPI‐Birds Network and Database (www.spibirds.org)—a large‐scale initiative that connects data from, and researchers working on, studies of wild populations of individually recognizable (usually ringed) birds. Within year and a half since the establishment, SPI‐Birds has recruited over 120 members, and currently hosts data on almost 1.5 million individual birds collected in 80 populations over 2,000 cumulative years, and counting.
    SPI‐Birds acts as a data hub and a catalogue of studied populations. It prevents data loss, secures easy data finding, use and integration and thus facilitates collaboration and synthesis. We provide community‐derived data and meta‐data standards and improve data integrity guided by the principles of Findable, Accessible, Interoperable and Reusable (FAIR), and aligned with the existing metadata languages (e.g. ecological meta‐data language).
    The encouraging community involvement stems from SPI‐Bird's decentralized approach: research groups retain full control over data use and their way of data management, while SPI‐Birds creates tailored pipelines to convert each unique data format into a standard format. We outline the lessons learned, so that other communities (e.g. those working on other taxa) can adapt our successful model. Creating community‐specific hubs (such as ours, COMADRE for animal demography, etc.) will aid much‐needed large‐scale ecological data integration.
    https://doi.org/10.1111/1365-2656.13388
  • 2021

    Efficient use of demographic data: integrated population models

    Marlène Gamelon, Stefan Vriend, Marcel E. Visser, Caspar A Hallmann, Suzanne T. E. Lommen, Eelke Jongejans
    Various types of demographic data can be collected in the field: population censuses, capture–mark–recapture data, and so on. These data sources share common demographic information about the studied population. Bayesian integrated population models (IPM) make efficient use of these different types of demographic data by jointly analysing them. This chapter discusses the advantages and the possibilities offered by this integrated approach. It describes the different steps required to build an IPM and illustrates the usefulness of this approach using two case studies. The first case study is a short-lived bird species, the blue tit, taking advantage of different data sources collected in a Dutch population to highlight how an integrated analysis might help to obtain a comprehensive picture of its dynamics. This IPM also assesses whether and how beech crop size might influence vital rates. The second case study is an invasive plant species, the common ragweed. The chapter illustrates how seedling data, plant data, and seed bank data could be analysed simultaneously to estimate key vital rates such as the probability that a seedling survives up to flowering.
    https://doi.org/10.1093/oso/9780198838609.003.0014
  • Frontiers in Ecology and Evolution
    2021

    Color of Artificial Light at Night Affects Incubation Behavior in the Great Tit, Parus major

    Artificial light at night (ALAN) has been recognized as a biodiversity threat due to the drastic effects it can have on many organisms. In wild birds, artificial illumination alters many natural behaviors that are important for fitness, including chick provisioning. Although incubation is a key determinant of the early developmental environment, studies into the effects of ALAN on bird incubation behavior are lacking. We measured nest temperature in nest boxes of great tits during the incubation period in two consecutive years. Nest boxes were located in eight previously dark field sites that have been experimentally illuminated since 2012 with white, green, or red light, or were left dark. We tested if light treatment affected mean nest temperature, number of times birds leave the nest (off-bout frequency), and off-bout duration during the incubation period. Subsequently, we investigated if incubation behavior is related to fitness. We found that birds incubating in the white light during a cold, early spring had lower mean nest temperatures at the end of incubation, both during the day and during the night, compared to birds in the green light. Moreover, birds incubating in white light took fewer off-bouts, but off-bouts were on average longer. The opposite was true for birds breeding in the green light. Low incubation temperatures and few but long off-bouts can have severe consequences for developing embryos. In our study, eggs from birds that took on average few off-bouts needed more incubation days to hatch compared to eggs from birds that took many off-bouts. Nevertheless, we found no clear fitness effects of light treatment or incubation behavior on the number of hatchlings or hatchling weight. Our results add to the growing body of literature that shows that effects of ALAN can be subtle, can differ due to the spectral composition of light, and can be year-dependent. These subtle alterations of natural behaviors might not have severe fitness consequences in the short-term. However, in the long term they could add up, negatively affecting parent condition and survival as well as offspring recruitment, especially in urban environments where more environmental pollutants are present.
    https://doi.org/10.3389/fevo.2021.728377
  • Scientific Reports
    27-10-2020

    Pollination and fruit infestation under artificial light at night: light colour matters

    Rapid human population growth and associated urbanization lead to increased artificial illumination of the environment. By changing the natural light–dark cycle, artificial lighting can affect the functioning of natural ecosystems. Many plants rely on insects in order to reproduce but these insects are known to be disturbed by artificial light. Therefore, plant–insect interactions may be affected when exposed to artificial illumination. These effects can potentially be reduced by using different light spectra than white light. We studied the effect of artificial lighting on plant–insect interactions in the Silene latifolia–Hadena bicruris system using a field set-up with four different light treatments: red, green, white and a dark control. We compared the proportion of fertilized flowers and fertilized ovules as well as the infestation of fruits by Hadena bicruris, a pollinating seed predator. We found no difference in the proportion of fertilized flowers among the treatments. The proportion of fruits infested by H. bicruris was however significantly higher under green and white light and a significantly lower proportion of fertilized ovules was found under green light. We show that artificial light with different colours impacts plant–insect interactions differently, with direct consequences for plant fitness.
    https://doi.org/10.1038/s41598-020-75471-1
  • Current Biology
    22-06-2020

    Experimental light at night has a negative long-term impact on macro-moth populations

    Roy H. A. van Grunsven, Jurriën R. van Deijk, Maurice Donners, Frank Berendse, Marcel E. Visser, Elmar M. Veenendaal, Kamiel Spoelstra
    Van Grunsven et al. experimentally test the long-term effects of artificial light on natural moth populations. In the initial two years there was no effect on populations, but in the latter three years population sizes were reduced compared with the dark controls. This shows that artificial light negatively affects moth populations.
    https://doi.org/10.1016/j.cub.2020.04.083
  • Nature Ecology and Evolution
    01-02-2020

    International scientists formulate a roadmap for insect conservation and recovery

    Jeff A. Harvey, Robin Heinen, Inge Armbrecht, Yves Basset, James H Baxter-Gilbert, T. Martijn Bezemer, Monika Böhm, Riccardo Bommarco, Paulo A V Borges, Pedro Cardoso, Viola Clausnitzer, Tara Cornelisse, Elizabeth E Crone, Marcel Dicke, Klaas-Douwe B Dijkstra, Lee A. Dyer, Jacintha Ellers, Thomas Fartmann, Matthew L. Forister, Michael J Furlong, Andres Garcia-Aguayo, Justin Gerlach, Rieta Gols, Dave Goulson, Jan-Christian Habel, Nick M Haddad, Caspar A Hallmann, Sérgio Henriques, Marie E Herberstein, Axel Hochkirch, Alice C Hughes, Sarina Jepsen, T Hefin Jones, Bora M Kaydan, David Kleijn, Alexandra-Maria Klein, Tanya Latty, Simon R Leather, Sara M Lewis, Bradford C Lister, John E Losey, Elizabeth C Lowe, Craig R Macadam, James Montoya-Lerma, Christopher D Nagano, Sophie Ogan, Michael C Orr, Christina J Painting, Thai-Hong Pham, Simon G. Potts, Aunu Rauf, Tomas L. Roslin, Michael J Samways, Francisco Sanchez-Bayo, Sim A Sar, Cheryl B Schultz, António O Soares, Anchana Thancharoen, Teja Tscharntke, Jason M. Tylianakis, Kate D L Umbers, Louise E.M. Vet, Marcel E. Visser, Ante Vujic, David L Wagner, Michiel F. WallisDeVries, Catrin Westphal, Thomas E White, Vicky L Wilkins, Paul H Williams, Kris A G Wyckhuys, Zeng-Rong Zhu, Hans de Kroon
    https://doi.org/10.1038/s41559-019-1079-8
  • Molecular Ecology
    01-02-2020

    Host dispersal shapes the population structure of a tick-borne bacterial pathogen

    Ana C. Norte, Gabriele Margos, Noemie S. Becker, Jaime Albino Ramos, Maria Sofia Nuncio, Volker Fingerle, Pedro Miguel Araujo, Peter Adamík, Haralambos Alivizatos, Emilio Barba, Rafael Barrientos, Laure Cauchard, Tibor Csörgő, Anastasia Diakou, N.J. Dingemanse, Blandine F. Doligez, Anna Dubiec, Tapio Eeva, Barbara Flaisz, Tomas Grim, Michaela Hau, D.J.A. Heylen, Sandor Hornok, Savas Kazantzidis, David Kovats, Frantisek Krause, Ivan Literak, Raivo Mänd, Lucia Mentesana, Jennifer Morinay, Marko Mutanen, Julio Manuel Neto, Marketa Novakova, Juan Jose Sanz, Luís P. da Silva, Hein Sprong, Ina-Sabrina Tirri, János Török, Tomi Trilar, Zdenek Tyller, Marcel E. Visser, Isabel Lopes de Carvalho
    Birds are hosts for several zoonotic pathogens. Because of their high mobility, especially of longdistance migrants, birds can disperse these pathogens, affecting their distribution and phylogeography. We focused on Borrelia burgdorferi sensu lato, which includes the causative agents of Lyme borreliosis, as an example for tick‐borne pathogens, to address the role of birds as propagation hosts of zoonotic agents at a large geographical scale. We collected ticks from passerine birds in 11 European countries. B . burgdorferi s.l. prevalence in Ixodes spp. was 37% and increased with latitude. The fieldfare Turdus pilaris and the blackbird T. merula carried ticks with the highest Borrelia prevalence (92 and 58%, respectively), whereas robin Erithacus rubecula ticks were the least infected (3.8%). Borrelia garinii was the most prevalent genospecies (61%), followed by B. valaisiana (24%), B. afzelii (9%), B. turdi (5%) and B. lusitaniae (0.5%). A novel Borrelia genospecies “Candidatus Borrelia aligera” was also detected. Multilocus sequence typing (MLST ) analysis of B. garinii isolates together with the global collection of B. garinii genotypes obtained from the Borrelia MLST public database revealed that: (a) there was little overlap among genotypes from different continents, (b) there was no geographical structuring within Europe, and (c) there was no evident association pattern detectable among B. garinii genotypes from ticks feeding on birds, questing ticks or human isolates. These findings strengthen the hypothesis that the population structure and evolutionary biology of tick‐borne pathogens are shaped by their host associations and the movement patterns of these hosts.
    https://doi.org/10.1111/mec.15336
  • Journal of Animal Ecology
    2020

    Comparing two measures of phenological synchrony in a predator–prey interaction: Simpler works better

    Jip Ramakers, Phillip Gienapp, Marcel E. Visser
    Abstract Global climate change has sparked a vast research effort into the demographic and evolutionary consequences of mismatches between consumer and resource phenology. Many studies have used the difference in peak dates to quantify phenological synchrony (match in dates, MD), but this approach has been suggested to be inconclusive, since it does not incorporate the temporal overlap between the phenological distributions (match in overlap, MO). We used 24 years of detailed data on the phenology of a predator?prey system, the great tit (Parus major) and the main food for its nestlings, caterpillars, to estimate MD and MO at the population and brood levels. We compared the performance of both metrics on two key demographic parameters: offspring recruitment probability and selection on the timing of reproduction. Although MD and MO correlated quadratically as expected, MD was a better predictor for both offspring recruitment and selection on timing than MO. We argue?and verify through simulations?that this is because quantifying MO has to be based on nontrivial, difficult-to-verify assumptions that likely render MO too inaccurate as a proxy for food availability in practice. Our results have important implications for the allocation of research efforts in long-term population studies in highly seasonal environments.
    https://doi.org/10.1111/1365-2656.13143
  • Nature Communications
    2020

    Meta-analysis of multidecadal biodiversity trends in Europe

    Francesca Pilotto, Ingolf Kühn, Rita Adrian, Renate Alber, Audrey Alignier, Christopher Andrews, Jaana Bäck, Luc Barbaro, Deborah Beaumont, Natalie Beenaerts, Sue Benham, David S. Boukal, Vincent Bretagnolle, Elisa Camatti, Roberto Canullo, Patricia G. Cardoso, B.J. Ens, Gert Everaert, Vesela Evtimova, Heidrun Feuchtmayr, Ricardo García-González, Daniel Gómez García, Ulf Grandin, Jerzy M. Gutowski, Liat Hadar, Lubos Halada, Melinda Halassy, Herman Hummel, Kaisa-Leena Huttunen, Bogdan Jaroszewicz, Thomas C. Jensen, Henrik Kalivoda, Inger K. Schmidt, Ingrid Kröncke, Reima Leinonen, Filipe Martinho, Henning Meesenburg, Julia Meyer, Stefano Minerbi, Don Monteith, Boris P. Nikolov, Daniel Oro, Dāvis Ozoliņš, Bachisio M. Padedda, Denise Pallett, Marco Pansera, Miguel Ângelo Pardal, Bruno Petriccione, Tanja Pipan, Juha Pöyry, Stefanie M. Schäfer, Marcus Schaub, Susanne C. Schneider, Agnija Skuja, Karline Soetaert, Gunta Spriņģe, Radoslav Stanchev, Jenni A. Stockan, Stefan Stoll, Lisa Sundqvist, Anne Thimonier, Gert Van Hoey, Gunther Van Ryckegem, Marcel E. Visser, Samuel Vorhauser, Peter Haase
    Local biodiversity trends over time are likely to be decoupled from global trends, as local processes may compensate or counteract global change. We analyze 161 long-term biological time series (15–91 years) collected across Europe, using a comprehensive dataset comprising ~6,200 marine, freshwater and terrestrial taxa. We test whether (i) local long-term biodiversity trends are consistent among biogeoregions, realms and taxonomic groups, and (ii) changes in biodiversity correlate with regional climate and local conditions. Our results reveal that local trends of abundance, richness and diversity differ among biogeoregions, realms and taxonomic groups, demonstrating that biodiversity changes at local scale are often complex and cannot be easily generalized. However, we find increases in richness and abundance with increasing temperature and naturalness as well as a clear spatial pattern in changes in community composition (i.e. temporal taxonomic turnover) in most biogeoregions of Northern and Eastern Europe.
    https://doi.org/10.1038/s41467-020-17171-y
  • Ecological Applications
    2020

    Artificial light at night, in interaction with spring temperature, modulates timing of reproduction in a passerine bird

    Davide Dominoni, Johan Kjellberg Jensen, Maaike de Jong, Marcel E. Visser, Kamiel Spoelstra
    Abstract The ecological impact of artificial light at night (ALAN) on phenological events such as reproductive timing is increasingly recognized. In birds, previous experiments under controlled conditions showed that ALAN strongly advances gonadal growth, but effects on egg-laying date are less clear. In particular, effects of ALAN on timing of egg-laying are found to be year-dependent, suggesting an interaction with climatic conditions such as spring temperature, which is known have strong effects on the phenology of avian breeding. Thus, we hypothesized that ALAN and temperature interact to regulate timing of reproduction in wild birds. Field studies have suggested that sources of ALAN rich in short wavelengths can lead to stronger advances in egg-laying date. We therefore tested this hypothesis in the great tit (Parus major), using a replicated experimental setup where eight previously unlit forest transects were illuminated with either white, green, or red LED light, or left dark as controls. We measured timing of egg-laying for 619 breeding events spread over six consecutive years and obtained temperature data for all sites and years. We detected overall significantly earlier egg-laying dates in the white and green light versus the dark treatment, and similar trends for red light. However, there was a strong inter-annual variability in mean egg-laying dates in all treatments, which was explained by spring temperature. We did not detect any fitness consequence of the changed timing of egg-laying due to ALAN, which suggests that advancing reproduction in response to ALAN might be adaptive.
    https://doi.org/10.1002/eap.2062
  • Proceedings of the National Academy of Sciences of the United States of America
    2020

    Fluctuating optimum and temporally variable selection on breeding date in birds and mammals

    Pierre de Villemereuil, Anne Charmantier, Debora Arlt, Pierre Bize, Patricia Brekke, Lyanne Brouwer, Andrew Cockburn, Steeve D Côté, F. Stephen Dobson, Simon R. Evans, Marco Festa-Bianchet, Marlène Gamelon, Sandra Hamel, Johann Hegelbach, Kurt Jerstad, Bart Kempenaers, L.E.B. Kruuk, Jouko Kumpula, Thomas Kvalnes, Andrew G. McAdam, S. Eryn McFarlane, Michael B. Morrissey, Tomas Pärt, Josephine M. Pemberton, Anna Qvarnström, Ole W Røstad, Julia Schroeder, Juan Carlos Senar, Ben C. Sheldon, Martijn van de Pol, Marcel E. Visser, Nathaniel T. Wheelwright, Jarle Tufto, Luis-Miguel Chevin
    Temporal variation in natural selection is predicted to strongly impact the evolution and demography of natural populations, with consequences for the rate of adaptation, evolution of plasticity, and extinction risk. Most of the theory underlying these predictions assumes a moving optimum phenotype, with predictions expressed in terms of the temporal variance and autocorrelation of this optimum. However, empirical studies seldom estimate patterns of fluctuations of an optimum phenotype, precluding further progress in connecting theory with observations. To bridge this gap, we assess the evidence for temporal variation in selection on breeding date by modeling a fitness function with a fluctuating optimum, across 39 populations of 21 wild animals, one of the largest compilations of long-term datasets with individual measurements of trait and fitness components. We find compelling evidence for fluctuations in the fitness function, causing temporal variation in the magnitude, but not the direction of selection. However, fluctuations of the optimum phenotype need not directly translate into variation in selection gradients, because their impact can be buffered by partial tracking of the optimum by the mean phenotype. Analyzing individuals that reproduce in consecutive years, we find that plastic changes track movements of the optimum phenotype across years, especially in bird species, reducing temporal variation in directional selection. This suggests that phenological plasticity has evolved to cope with fluctuations in the optimum, despite their currently modest contribution to variation in selection.
    https://doi.org/10.1073/pnas.2009003117
  • Environmental Pollution
    2020

    Multisensory pollution: Artificial light at night and anthropogenic noise have interactive effects on activity patterns of great tits (Parus major)

    Davide Dominoni, Judith Smit, Marcel E. Visser, Wouter Halfwerk
    Urbanisation is increasing globally at a rapid pace. Consequently, wild species face novel environmental stressors associated with urban sprawl, such as artificial light at night and noise. These stressors have pervasive effects on the behaviour and physiology of many species. Most studies have singled out the impact of just one of these stressors, while in the real world they are likely to co-occur both temporally and spatially, and we thus lack a clear understanding of the combined effect of anthropogenic stressors on wild species. Here, we experimentally exposed captive male great tits (Parus major) to artificial light at night and 24 h noise in a fully factorial experiment. We then measured the effect of both these stressors on their own and their combination on the amount and timing of activity patterns. We found that both light and noise affected activity patterns when presented alone, but in opposite ways: light increased activity, particularly at night, while noise reduced it, particularly during the day. When the two stressors were combined, we found a synergistic effect on the total activity and the nighttime activity, but an antagonistic effect on daytime activity. The significant interaction between noise and light treatment also differed among forest and city birds. Indeed, we detected a significant interactive effect on light and noise on daytime, nighttime, dusktime and offset of activity of urban birds, but not of forest birds. These results suggest that both artificial light at night and anthropogenic noise can drive changes in activity patterns, but that the specific impacts depend on the habitat of origin. Furthermore, our results demonstrate that co-occurring exposure to noise and light can lead to a stronger impact at night than predicted from the additive effects and thus that multisensory pollution may be a considerable threat for wildlife.
    https://doi.org/10.1016/j.envpol.2019.113314
  • Journal of Evolutionary Biology
    2020

    Quantifying individual variation in reaction norms: Mind the residual

    Jip Ramakers, Marcel E. Visser, Phillip Gienapp
    Abstract Phenotypic plasticity is a central topic in ecology and evolution. Individuals may differ in the degree of plasticity (individual-by-environment interaction (I ? E)), which has implications for the capacity of populations to respond to selection. Random regression models (RRMs) are a popular tool to study I ? E in behavioural or life-history traits, yet evidence for I ? E is mixed, differing between species, populations, and even between studies on the same population. One important source of discrepancies between studies is the treatment of heterogeneity in residual variance (heteroscedasticity). To date, there seems to be no collective awareness among ecologists of its influence on the estimation of I ? E or a consensus on how to best model it. We performed RRMs with differing residual variance structures on simulated data with varying degrees of heteroscedasticity and plasticity, sample size and environmental variability to test how RRMs would perform under each scenario. The residual structure in the RRMs affected the precision of estimates of simulated I ? E as well as statistical power, with substantial lack of precision and high false-positive rates when sample size, environmental variability and plasticity were small. We show that model comparison using information criteria can be used to choose among residual structures and reinforce this point by analysis of real data of two study populations of great tits (Parus major). We provide guidelines that can be used by biologists studying I ? E that, ultimately, should lead to a reduction in bias in the literature concerning the statistical evidence and the reported magnitude of variation in plasticity.
    https://doi.org/10.1111/jeb.13571
  • Journal of Experimental Biology
    2020

    Temperature has a causal and plastic effect on timing of breeding in a small songbird

    Irene C. Verhagen, Barbara Tomotani, Phillip Gienapp, Marcel E. Visser
    Phenotypic plasticity is an important mechanism by which an individual can adapt its seasonal timing to predictable, short-term environmental changes by using predictive cues. Identification of these cues is crucial to forecast the response of species to long-term environmental change and to study their potential to adapt. Individual great tits (Parus major) start reproduction early under warmer conditions in the wild, but whether this effect is causal is not well known. We housed 36 pairs of great tits in climate-controlled aviaries and 40 pairs in outdoor aviaries, where they bred under artificial contrasting temperature treatments or in semi-natural conditions, respectively, for two consecutive years, using birds from lines selected for early and late egg laying. We thus obtained laying dates in two different thermal environments for each female. Females bred earlier under warmer conditions in climate-controlled aviaries, but not in outdoor aviaries. The latter was inconsistent with laying dates from our wild population. Further, early selection line females initiated egg laying consistently 9 days earlier than late selection line females in outdoor aviaries, but we found no difference in the degree of plasticity (i.e. the sensitivity to temperature) in laying date between selection lines. Because we found that temperature causally affects laying date, climate change will lead to earlier laying. This advancement is, however, unlikely to be sufficient, thereby leading to selection for earlier laying. Our results suggest that natural selection may lead to a change in mean phenotype, but not to a change in the sensitivity of laying dates to temperature.
    https://doi.org/10.1242/jeb.218784
  • BMC Genomics
    02-09-2019

    Exploration of tissue-specific gene expression patterns underlying timing of breeding in contrasting temperature environments in a song bird

    Veronika Laine, Irene C. Verhagen, A.C. Mateman, Agata Pijl, Tony D. Williams, Phillip Gienapp, Kees van Oers, Marcel E. Visser
    Seasonal timing of breeding is a life history trait with major fitness consequences but the genetic basis of the physiological mechanism underlying it, and how gene expression is affected by date and temperature, is not well known. In order to study this, we measured patterns of gene expression over different time points in three different tissues of the hypothalamic-pituitary-gonadal-liver axis, and investigated specifically how temperature affects this axis during breeding. We studied female great tits (Parus major) from lines artificially selected for early and late timing of breeding that were housed in two contrasting temperature environments in climate-controlled aviaries. We collected hypothalamus, liver and ovary samples at three different time points (before and after onset of egg-laying). For each tissue, we sequenced whole transcriptomes of 12 pools (n = 3 females) to analyse gene expression.
    https://doi.org/10.1186/s12864-019-6043-0
  • Journal of Experimental Biology
    01-09-2019

    Timing manipulations reveal the lack of a causal link across timing of annual-cycle stages in a long-distance migrant

    Barbara Tomotani, Iván De la Hera, Cynthia Lange, Bart van Lith, Simone L. Meddle, Christiaan Both, Marcel E. Visser
    Organisms need to time their annual-cycle stages, like breeding and migration, to occur at the right time of the year. Climate change has shifted the timing of annual-cycle stages at different rates, thereby tightening or lifting time constraints of these annual-cycle stages, a rarely studied consequence of climate change. The degree to which these constraints are affected by climate change depends on whether consecutive stages are causally linked (scenario I) or whether the timing of each stage is independent of other stages (scenario II). Under scenario I, a change in timing in one stage has knock-on timing effects on subsequent stages, whereas under scenario II, a shift in the timing of one stage affects the degree of overlap with previous and subsequent stages. To test this, we combined field manipulations, captivity measurements and geolocation data. We advanced and delayed hatching dates in pied flycatchers (Ficedula hypoleuca) and measured how the timing of subsequent stages (male moult and migration) were affected. There was no causal effect of manipulated hatching dates on the onset of moult and departure to Africa. Thus, advancing hatching dates reduced the male moult–breeding overlap with no effect on the moult–migration interval. Interestingly, the wintering location of delayed males was more westwards, suggesting that delaying the termination of breeding carries over to winter location. Because we found no causal linkage of the timing of annual-cycle stages, climate change could shift these stages at different rates, with the risk that the time available for some becomes so short that this will have major fitness consequences.
    https://doi.org/10.1242/jeb.201467
  • Methods in Ecology and Evolution
    01-09-2019

    A time-series model for estimating temporal variation in phenotypic selection on laying dates in a Dutch great tit population

    Yihan Cao, Marcel E. Visser, Jarle Tufto
    Abstract Temporal and spatial variation in phenotypic selection due to changing environmental conditions is of great interest to evolutionary biologists, but few existing methods estimating its magnitude take into account the temporal autocorrelation. We use state-space models (SSMs) to analyse phenotypic selection processes that cannot be observed directly and use Template Model builder (TMB), an R package for computing and maximizing the Laplace approximation of the marginal likelihood for SSM and other complex, nonlinear latent variable model via automatic differentiation. Using a long-term great tit (Parus major) dataset, we fit several SSMs and conduct model selection based on Akaike information criterion (AIC) to assess the support for fluctuated directional or autocorrelated stabilizing selection on breeding time of the great tit population. Our results show that there is directional selection on the probability of breeding failure, and stabilizing selection on the mean number of fledglings. This selection for early laying date is consistent with a previous study of the same population. We also estimate the variation and autocorrelation in other parameters of the fitness functions, including the width and height, and found the height and location of annual fitness function are autocorrelated with significant variation, while the width can be assumed to constant over time. Using TMB to fit SSMs, we are able to estimate additional parameters compared to previous methods, all without requiring a substantial increase in computational resources. Furthermore, our specification of complex nonlinear model structure benefits greatly from the flexibility of model formulation with TMB. Therefore, our approach could be directly applied to estimating even more complicated phenotypic selection processes induced by environmental change for other species.
    https://doi.org/10.1111/2041-210X.13249
  • Journal of Experimental Biology
    07-2019

    Short-term, but not long-term, increased daytime workload leads to decreased night-time energetics in a free-living song bird

    Marcel E. Visser, Coby van Dooremalen, Barbara Tomotani, Andrey Bushuev, Harro A. J. Meijer, Luc te Marvelde, Phillip Gienapp
    Reproduction is energetically expensive and to obtain sufficient energy, animals can either alter their metabolic system over time to increase energy intake (increased-intake hypothesis) or reallocate energy from maintenance processes (compensation hypothesis). The first hypothesis predicts a positive relationship between basal metabolic rate (BMR) and energy expenditure (DEE) because of the higher energy demands of the metabolic system at rest. The second hypothesis predicts a trade-off between different body functions, with a reduction of the BMR as a way to compensate for increased daytime energetic expenditure. We experimentally manipulated the workload of wild pied flycatchers by adding or removing chicks when chicks were 2 and 11 days old. We then measured the feeding frequency (FF), DEE and BMR at day 11, allowing us to assess both short- and long-term effects of increased workload. The manipulation at day 2 caused an increase in FF when broods were enlarged, but no response in DEE or BMR, while the manipulation at day 11 caused an increase in FF, no change in DEE and a decrease in BMR in birds with more chicks. Our results suggest that pied flycatchers adjust their workload but that this does not lead to a higher BMR at night (no support for the increased-intake hypothesis). In the short term, we found that birds reallocate energy with a consequent reduction of BMR (evidence for the compensation hypothesis). Birds thus resort to short-term strategies to increase energy expenditure, which could explain why energy expenditure and hard work are not always correlated in birds.
    https://doi.org/10.1242/jeb.199513
  • Evolution Letters
    01-06-2019

    Response to Perrier and Charmantier: On the importance of time scales when studying adaptive evolution

    Mirte Bosse, Lewis G. Spurgin, Veronika Laine, Ella F. Cole, Josh A. Firth, Phillip Gienapp, Andrew G. Gosler, Keith McMahon, Jocelyn Poissant, Irene C. Verhagen, Martien A.M. Groenen, Kees van Oers, Ben C. Sheldon, Marcel E. Visser, Jon Slate
    https://doi.org/10.1002/evl3.112
  • Proceedings of the Royal Society B-Biological Sciences
    15-05-2019

    Personality and gonadal development as sources of individual variation in response to GnRH challenge in female great tits

    Samuel P. Caro, Charlotte A Cornil, Kees van Oers, Marcel E. Visser

    Seasonal timing of reproduction is a key life-history trait, but we know little about the mechanisms underlying individual variation in female endocrine profiles associated with reproduction. In birds, 17β-oestradiol is a key reproductive hormone that links brain neuroendocrine mechanisms, involved in information processing and decision-making, to downstream mechanisms in the liver, where egg-yolk is produced. Here, we test, using a simulated induction of the reproductive system through a Gonadotropin-Releasing Hormone (GnRH) challenge, whether the ovary of pre-breeding female great tits responds to brain stimulation by increasing oestradiol. We also assess how this response is modified by individual-specific traits like age, ovarian follicle size, and personality, using females from lines artificially selected for divergent levels of exploratory behaviour. We show that a GnRH injection leads to a rapid increase in circulating concentrations of oestradiol, but responses varied among individuals. Females with more developed ovarian follicles showed stronger responses and females from lines selected for fast exploratory behaviour showed stronger increases compared to females from the slow line, indicating a heritable component. This study shows that the response of the ovary to reproductive stimulation from the brain greatly varies among individuals and that this variation can be attributed to several commonly measured individual traits, which sheds light on the mechanisms shaping heritable endocrine phenotypes.

    https://doi.org/10.1098/rspb.2019.0142
  • Genome Biology and Evolution
    01-05-2019

    The Genomic Complexity of a Large Inversion in Great Tits

    Vinicius Henrique da Silva, Veronika Laine, Mirte Bosse, Lewis G. Spurgin, Martijn Derks, Kees van Oers, Bert W. Dibbits, Jon Slate, Richard P.M.A Crooijmans, Marcel E. Visser, Martien A.M. Groenen
    Chromosome inversions have clear effects on genome evolution and have been associated with speciation, adaptation, and the evolution of the sex chromosomes. In birds, these inversions may play an important role in hybridization of species and disassortative mating. We identified a large (\64\ Mb) inversion polymorphism in the great tit (Parus major) that encompasses almost 1,000 genes and more than 90\% of Chromosome 1A. The inversion occurs at a low frequency in a set of over 2,300 genotyped great tits in the Netherlands with only 5\% of the birds being heterozygous for the inversion. In an additional analysis of 29 resequenced birds from across Europe, we found two heterozygotes. The likely inversion breakpoints show considerable genomic complexity, including multiple copy number variable segments. We identified different haplotypes for the inversion, which differ in the degree of recombination in the center of the chromosome. Overall, this remarkable genetic variant is widespread among distinct great tit populations and future studies of the inversion haplotype, including how it affects the fitness of carriers, may help to understand the mechanisms that maintain it.
    https://doi.org/10.1093/gbe/evz106
  • Evolution Letters
    01-04-2019

    Genomic selection on breeding time in a wild bird population

    Phillip Gienapp, Mario P. L. Calus, Veronika Laine, Marcel E. Visser
    Abstract Artificial selection experiments are a powerful tool in evolutionary biology. Selecting individuals based on multimarker genotypes (genomic selection) has several advantages over phenotype-based selection but has, so far, seen very limited use outside animal and plant breeding. Genomic selection depends on the markers tagging the causal loci that underlie the selected trait. Because the number of necessary markers depends, among other factors, on effective population size, genomic selection may be in practice not feasible in wild populations as most wild populations have much higher effective population sizes than domesticated populations. However, the current possibilities of cost-effective high-throughput genotyping could overcome this limitation and thereby make it possible to apply genomic selection also in wild populations. Using a unique dataset of about 2000 wild great tits (Parus major), a small passerine bird, genotyped on a 650 k SNP chip we calculated genomic breeding values for egg-laying date using the so-called GBLUP approach. In this approach, the pedigree-based relatedness matrix of an ?animal model,? a special form of the mixed model, is replaced by a marker-based relatedness matrix. Using the marker-based relatedness matrix, the model seemed better able to disentangle genetic and permanent environmental effects. We calculated the accuracy of genomic breeding values by correlating them to the phenotypes of individuals whose phenotypes were excluded from the analysis when estimating the genomic breeding values. The obtained accuracy was about 0.20, with very little effect of the used genomic relatedness estimator but a strong effect of the number of SNPs. The obtained accuracy is lower than typically seen in domesticated species but considerable for a trait with low heritability (?0.2) as avian breeding time. Our results show that genomic selection is possible also in wild populations with potentially many applications, which we discuss here.
    https://doi.org/10.1002/evl3.103
  • Genome Biology and Evolution
    06-03-2019

    Seasonal Variation in Genome-Wide DNA Methylation Patterns and the Onset of Seasonal Timing of Reproduction in Great Tits

    Heidi M. Viitaniemi, Irene C. Verhagen, Marcel E. Visser, Antti Honkela, Kees van Oers, Arild Husby
    In seasonal environments, timing of reproduction is a trait with important fitness consequences, but we know little about the molecular mechanisms that underlie the variation in this trait. Recently, several studies put forward DNA methylation as a mechanism regulating seasonal timing of reproduction in both plants and animals. To understand the involvement of DNA methylation in seasonal timing of reproduction, it is necessary to examine within-individual temporal changes in DNA methylation, but such studies are very rare. Here, we use a temporal sampling approach to examine changes in DNA methylation throughout the breeding season in female great tits (Parus major) that were artificially selected for early timing of breeding. These females were housed in climate-controlled aviaries and subjected to two contrasting temperature treatments. Reduced representation bisulfite sequencing on red blood cell derived DNA showed genome-wide temporal changes in more than 40,000 out of the 522,643 CpG sites examined. Although most of these changes were relatively small (mean within-individual change of 6%), the sites that showed a temporal and treatment-specific response in DNA methylation are candidate sites of interest for future studies trying to understand the link between DNA methylation patterns and timing of reproduction.
    https://doi.org/10.1093/gbe/evz044
  • BMC Genomics
    08-01-2019

    Exploring the unmapped DNA and RNA reads in a songbird genome

    Veronika Laine, Toni I. Gossmann, Kees van Oers, Marcel E. Visser, Martien A.M. Groenen

    BACKGROUND: A widely used approach in next-generation sequencing projects is the alignment of reads to a reference genome. Despite methodological and hardware improvements which have enhanced the efficiency and accuracy of alignments, a significant percentage of reads frequently remain unmapped. Usually, unmapped reads are discarded from the analysis process, but significant biological information and insights can be uncovered from these data. We explored the unmapped DNA (normal and bisulfite treated) and RNA sequence reads of the great tit (Parus major) reference genome individual. From the unmapped reads we generated de novo assemblies, after which the generated sequence contigs were aligned to the NCBI non-redundant nucleotide database using BLAST, identifying the closest known matching sequence.

    RESULTS: Many of the aligned contigs showed sequence similarity to different bird species and genes that were absent in the great tit reference assembly. Furthermore, there were also contigs that represented known P. major pathogenic species. Most interesting were several species of blood parasites such as Plasmodium and Trypanosoma.

    CONCLUSIONS: Our analyses revealed that meaningful biological information can be found when further exploring unmapped reads. For instance, it is possible to discover sequences that are either absent or misassembled in the reference genome, and sequences that indicate infection or sample contamination. In this study we also propose strategies to aid the capture and interpretation of this information from unmapped reads.

    https://doi.org/10.1186/s12864-018-5378-2
  • Scientific data
    2019

    Temporally replicated reduced representation bisulfate sequencing data on DNA methylation patterns in great tit.

    Hannu Mäkinen, Heidi M. Viitaniemi, Marcel E. Visser, Irene C. Verhagen, Kees van Oers, Arild Husby
    Seasonal timing of reproduction is an important fitness trait in many plants and animals but the underlying molecular mechanism for this trait is poorly known. DNA methylation is known to affect timing of reproduction in various organisms and is therefore a potential mechanism also in birds. Here we describe genome wide data aiming to detect temporal changes in methylation in relation to timing of breeding using artificial selection lines of great tits (Parus major) exposed to contrasting temperature treatments. Methylation levels of DNA extracted from erythrocytes were examined using reduced representation bisulfite sequencing (RRBS). In total, we obtained sequencing data from 63 libraries over four different time points from 16 birds with on average 20 million quality filtered reads per library. These data describe individual level temporal variation in DNA methylation throughout the breeding season under experimental temperature regimes and provides a resource for future studies investigating the role of temporal changes in DNA methylation in timing of reproduction.
    https://doi.org/10.1038/s41597-019-0136-0
  • Evolution
    2019

    Phenological mismatch drives selection elevation, but not on slope, of breeding time plasticity in a wild songbird

    Jip Ramakers, Phillip Gienapp, Marcel E. Visser
    Phenotypic plasticity is an important mechanism for populations to respond to fluctuating environments, yet may be insufficient to adapt to a directionally changing environment. To study whether plasticity can evolve under current climate change, we quantified selection and genetic variation in both the elevation (RNE) and slope (RNS) of the breeding time reaction norm in a long‐term (1973–2016) study population of great tits (Parus major). The optimal RNE (the caterpillar biomass peak date regressed against the temperature used as cue by great tits) changed over time, whereas the optimal RNS did not. Concordantly, we found strong directional selection on RNE, but not RNS, of egg‐laying date in the second third of the study period; this selection subsequently waned, potentially due to increased between‐year variability in optimal laying dates. We found individual and additive genetic variation in RNE but, contrary to previous studies on our population, not in RNS. The predicted and observed evolutionary change in RNE were, however, marginal, due to low heritability and the sex limitation of laying date. We conclude that adaptation to climate change can only occur via micro‐evolution of RNE, but this will necessarily be slow and potentially hampered by increased variability in phenotypic optima.
    https://doi.org/10.1111/evo.13660
  • Nature Ecology and Evolution
    2019

    Evolutionary and demographic consequences of phenological mismatches

    Marcel E. Visser, Phillip Gienapp
    Climate change has often led to unequal shifts in the seasonal timing (phenology) of interacting species, such as consumers and their resource, leading to phenological ‘mismatches’. Mismatches occur when the time at which a consumer species’s demands for a resource are high does not match with the period when this resource is abundant. Here, we review the evolutionary and population-level consequences of such mismatches and how these depend on other ecological factors, such as additional drivers of selection and density-dependent recruitment. This review puts the research on phenological mismatches into a conceptual framework, applies this framework beyond consumer–resource interactions and illustrates this framework using examples drawn from the vast body of literature on mismatches. Finally, we point out priority questions for research on this key impact of climate change.
    https://doi.org/10.1038/s41559-019-0880-8
  • Nature Communications
    2019

    Adaptive responses of animals to climate change are most likely insufficient

    Viktoriia Radchuk, Thomas Reed, Céline Teplitsky, Martijn van de Pol, Anne Charmantier, Christopher Hassall, Peter Adamík, Frank Adriaensen, Markus P. Ahola, Peter Arcese, Jesús Miguel Avilés, Javier Balbontín, Karl S. Berg, Antoni Borras, Sarah J. Burthe, Jean Clobert, Nina Dehnhard, Florentino de Lope, André A Dhondt, N.J. Dingemanse, Hideyuki Doi, Tapio Eeva, Joerns Fickel, Iolanda Filella, Frode Fossøy, Anne E. Goodenough, Stephen J. G. Hall, Bengt Hansson, Michael P. Harris, Dennis Hasselquist, Thomas Hickler, Jasmin Joshi, Heather Kharouba, Juan Gabriel Martínez, Jean-Baptiste Mihoub, James A Mills, Mercedes Molina-Morales, Arne Moksnes, arpat ozgul, Deseada Parejo, Philippe Pilard, Maud Poisbleau, Francois Rousset, Mark-Oliver Rödel, David Scott, Juan Carlos Senar, Constanti Stefanescu, Bård G. Stokke, Tamotsu Kusano, Maja Tarka, Corey E. Tarwater, Kirsten Thonicke, Jack Thorley, Andreas Wilting, Piotr Tryjanowski, Juha Merilä, Ben C. Sheldon, Anders P. Møller, Erik Matthysen, Fredric Janzen, F. Stephen Dobson, Marcel E. Visser, Steven R. Beissinger, Alexandre Courtiol, Stephanie Kramer-Schadt
    Biological responses to climate change have been widely documented across taxa and regions, but it remains unclear whether species are maintaining a good match between phenotype and environment, i.e. whether observed trait changes are adaptive. Here we reviewed 10,090 abstracts and extracted data from 71 studies reported in 58 relevant publications, to assess quantitatively whether phenotypic trait changes associated with climate change are adaptive in animals. A meta-analysis focussing on birds, the taxon best represented in our dataset, suggests that global warming has not systematically affected morphological traits, but has advanced phenological traits. We demonstrate that these advances are adaptive for some species, but imperfect as evidenced by the observed consistent selection for earlier timing. Application of a theoretical model indicates that the evolutionary load imposed by incomplete adaptive responses to ongoing climate change may already be threatening the persistence of species.
    https://doi.org/10.1038/s41467-019-10924-4
  • Current Biology
    2019

    Evolution: Adapting to a Warming World

    Summary To be able to cope with climate change, species need to evolve. Demonstrating such evolution in wild populations is notoriously difficult. Replication of a 21-year-old experiment demonstrates that a long-distance migratory songbird has genetically adapted to climate change.
    https://doi.org/10.1016/j.cub.2019.09.062
  • Journal of Avian Biology
    2019

    Manipulation of photoperiod perception advances gonadal growth but not laying date in the great tit

    Lucia Salis, Samuel P. Caro, Roelof A Hut, Louis Vernooij, Marcel E. Visser
    In seasonal environments, organisms use biotic and abiotic cues to time various biological processes that are crucial for growth, survival and reproductive success. Photoperiod is the best-known cue used to regulate gonadal development, migration and moult of many animal species. In birds, the relationship between photoperiod and gonadal development is clearly established, but we have little understanding on whether photoperiod also regulates actual timing of egg laying under natural conditions. Elucidating the link between photoperiod and timing of breeding is however key to understand whether an evolutionary change in sensitivity to photoperiod is a possible mechanism through which organisms could adjust their seasonal timing in response to climate warming. Here, we investigated the causal relationship between photoperiod, gonadal growth and laying date in wild female great tits. We experimentally increased the photoperiod perceived by the birds in spring by clipping head feathers, and we subsequently monitored gonadal development in the lab and egg laying dates in the wild. We show that our manipulation increased the photoperiod perceived by the birds to a level that approximately corresponds to an advancement of ten calendar days. This increase in perceived photoperiod led to an acceleration of gonadal development, but not to an advancement of egg laying dates. Our results indicate that photoperiod sensitivity is not constraining the advancement of laying date under current environmental conditions and suggest that evolution of sensitivity to other supplementary cues is necessary to advance reproduction under global warming. This article is protected by copyright. All rights reserved.
    https://doi.org/10.1111/jav.02197
  • American Naturalist
    2019

    Between- and within-individual variation of maternal thyroid hormone deposition in wild great tits (Parus major)

    Bin-Yan Hsu, Irene C. Verhagen, Phillip Gienapp, Veerle M. Darras, Marcel E. Visser, Suvi Ruuskanen
    Maternal hormones are often considered a mediator of anticipatory maternal effects, namely mothers adjust maternal hormone transfer to prepare the offspring for the anticipated environment. The flexibility for mothers to adjust hormone transfer is therefore a prerequisite for such anticipatory maternal effects. Nevertheless, previous studies only focused on the average differences of maternal hormone transfer between groups and neglected the substantial individual variation, despite that individual plasticity on maternal hormone transfer is actually the central assumption. In this study, we studied the between- and within-individual variation of maternal thyroid hormones (THs) in egg yolk of wild great tits (Parus major) and estimated the individual plasticity of maternal yolk THs across environmental temperature, clutch initiation dates and egg laying order using linear mixed-effects models. Interestingly, our models provide statistical evidence that the two main THs – the main biologically active hormone T3, and the prohormone T4 – exhibited different variation patterns. Yolk T3 showed significant between-individual variation on the average levels, in line with its previously reported moderate heritability. Yolk T4, however, showed significant between-clutch variation in the pattern over the laying sequence, suggesting a great within-individual plasticity. Our findings suggest that the role and function of the hormone (pro vs active hormone) within the endocrine axis likely influences its flexibility to respond to environmental change. Whether the flexibility of T4 deposition brings fitness advantage should be examined along with its potential effects on offspring, which remains to be further investigated.
    https://doi.org/10.1086/704738
  • Journal of Experimental Biology
    2019

    Fine-tuning of seasonal timing of breeding is regulated downstream in the underlying neuro-endocrine system in a small songbird

    Irene C. Verhagen, Veronika Laine, A.C. Mateman, Agata Pijl, Ruben de Wit, Bart van Lith, W. Kamphuis, Heidi M. Viitaniemi, Tony D. Williams, Samuel P. Caro, Simone L. Meddle, Phillip Gienapp, Kees van Oers, Marcel E. Visser
    Timing of breeding is under selection in wild populations due to climate change, and understanding the underlying physiological processes mediating timing provides insight in the potential rate of adaptation. Current knowledge on this variation in physiology is, however, mostly limited to males. We assessed whether individual differences in timing of breeding in females are reflected in differences in candidate gene expression and if so, whether these differences occur in the upstream (hypothalamus), or downstream (ovary and liver) parts of the neuroendocrine system. We used 72 female great tits from two generations of lines artificially selected for early and late egg-laying, which were housed in climate controlled aviaries and went through two breeding cycles within one year. In the first breeding season we obtained individual egg-laying dates, while in the second breeding season, using the same individuals, we sampled several tissues at three time points based on timing of the first breeding attempt. For each tissue, mRNA expression levels were measured using qPCR for a set of candidate genes associated with timing of reproduction and subsequently analysed for differences between generations, time points and individual timing of breeding. We found differences in gene expression between generations in all tissues with most pronounced differences in the hypothalamus. Differences between time points, and early and late laying females, were found exclusively in ovary and liver. Altogether, we show that fine-tuning of seasonal timing of breeding, and thereby the opportunity for adaptation in the neuroendocrine system, is regulated mostly downstream in the neuro-endocrine system.
    https://doi.org/10.1242/jeb.202481
  • Proceedings of the Royal Society B-Biological Sciences
    2019

    The preference and costs of sleeping under light at night in forest and urban great tits

    Zeynep Ulgezen, Teemu Käpylä, Peter Meerlo, Kamiel Spoelstra, Marcel E. Visser, Davide Dominoni
    Artificial light at night (ALAN) is an increasing phenomenon associated with worldwide urbanization. In birds, broad-spectrum white ALAN can have disruptive effects on activity patterns, metabolism, stress response and immune function. There has been growing research on whether the use of alternative light spectra can reduce these negative effects, but surprisingly, there has been no study to determine which light spectrum birds prefer. To test such a preference, we gave urban and forest great tits (Parus major) the choice where to roost using pairwise combinations of darkness, white light or green dim light at night (1.5 lux). Birds preferred to sleep under artificial light instead of darkness, and green was preferred over white light. In a subsequent experiment, we investigated the consequence of sleeping under a particular light condition, and measured birds' daily activity levels, daily energy expenditure (DEE), oxalic acid as a biomarker for sleep debt and cognitive abilities. White light affected activity patterns more than green light. Moreover, there was an origin-dependent response to spectral composition: in urban birds, the total daily activity and night activity did not differ between white and green light, while forest birds were more active under white than green light. We also found that individuals who slept under white and green light had higher DEE. However, there were no differences in oxalic acid levels or cognitive abilities between light treatments. Thus, we argue that in naive birds that had never encountered light at night, white light might disrupt circadian rhythms more than green light. However, it is possible that the negative effects of ALAN on sleep and cognition might be observed only under intensities higher than 1.5 lux. These results suggest that reducing the intensity of light pollution as well as tuning the spectrum towards long wavelengths may considerably reduce its impact.
    https://doi.org/10.1098/rspb.2019.0872
  • Functional Ecology
    2019

    Genetic and phenotypic responses to genomic selection for timing of breeding in a wild songbird

    Irene C. Verhagen, Phillip Gienapp, Veronika Laine, Elizabeth van Grevenhof, A.C. Mateman, Kees van Oers, Marcel E. Visser
    The physiological mechanisms underlying avian seasonal timing of reproduction, a life‐history trait with major fitness consequences, are not well understood. Comparing individuals that have been selected to differ in their timing of breeding may prove to be a promising in studying these mechanisms, making selection lines a valuable tool.
    We created selection lines for early and late timing of breeding in great tits (Parus major) using genomic selection, that is selection based on multi‐marker genotypes rather than on the phenotype. We took in nestlings (F1 generation) from wild broods of which the mother was either an extremely early (“early line”) or extremely late (“late line”) breeder. These chicks were then genotyped and, based on their “genomic breeding values” (GEBVs), we selected individuals for early and late line breeding pairs to produce the F2 generation in captivity. The F2 offspring was hand‐reared, genotyped and selected to produce an F3 generation, which were then again genotyped and selected. This way we obtained laying dates in aviaries for F1, F2 and F3 birds.
    We studied the genetic response to the artificial selection and found increased genetic differentiation between the early and late reproducing selection lines over generations (F1–F3), indicated by both diverging GEBVs and increased fixation indices (FST).
    We studied the phenotypic response to selection for birds breeding in outdoor breeding aviaries. We found that early line birds laid earlier than late line birds, and this difference increased over the generations (F1–F3), with non‐significant line effects for the F1 and F2, but highly significant line differences for the F3.
    We also assessed whether there was correlated selection on two traits that are potentially part of the mechanisms underlying seasonal timing: the endogenous free‐running period of the day/night clock (tau) and basal metabolic rate, but found no correlated selection.
    We have successfully created selection lines on seasonal timing in a wild bird species and obtained an instrument for future studies to investigate the physiological mechanisms underlying timing of breeding, and the genetic variation in these mechanisms, an essential component for evolutionary change in timing of reproduction.
    https://doi.org/10.1111/1365-2435.13360
  • Frontiers in Ecology and Evolution
    2019

    The Genomics of Circadian Timing in a Wild Bird, the Great Tit (Parus major)

    Veronika Laine, Els Atema, Priscilla Vlaming, Irene C. Verhagen, A.C. Mateman, Jip Ramakers, Kees van Oers, Kamiel Spoelstra, Marcel E. Visser
    Circadian rhythms are ubiquitous among taxa and are essential for coping with recurrent daily events, leading to selection on the properties of the clock underlying these rhythms. To quantify this selection in the wild, we need, however, to phenotype wild individuals, which is difficult using the standard laboratory approach for which individuals need to be kept under constant conditions. To overcome this problem, we explored the possibility to link the variation in a key clock property, circadian period (Tau), to genetic variation. We measured Tau in 152 captive great tits (Parus major). We further linked Tau to two circadian phase markers, the onset of activity in the Light:Dark cycle, and the first onset in constant conditions (Dim:Dim), directly after entrainment. We did a genome-wide association study using a 650k SNP chip, and we linked genetic polymorphisms of a set of twelve candidate genes, to Tau and the two circadian phase markers. In line with earlier studies, Tau was heritable (h2 =0.48 ± 0.22). Despite this genetic variation, we did not find any significant associations at the genome-wide level with the measured traits and only one candidate gene showed association with onset of activity in the Light:Dark cycle. Identifying the genetic base of circadian timing for wild species thus remains challenging. Including alternative molecular methods such as epigenetics or transcriptomics could help to unravel the molecular basis of the biological clock in great tits.
    https://doi.org/10.3389/fevo.2019.00152
  • Ecology and Evolution
    12-2018

    Interspecific transfer of parasites following a range-shift in Ficedula flycatchers

    William Jones, Katarzyna Kulma, Staffan Bensch, Mariusz Cichoń, Anvar B. Kerimov, Miloš Krist, Toni Laaksonen, Juan Moreno, Pavel Munclinger, Fred M. Slater, Eszter Szöllősi, Marcel E. Visser, Anna Qvarnström
    Human-induced climate change is expected to cause major biotic changes in species distributions and thereby including escalation of novel host-parasite associations. Closely related host species that come into secondary contact are especially likely to exchange parasites and pathogens. Both the Enemy Release Hypothesis (where invading hosts escape their original parasites) and the Novel Weapon Hypothesis (where invading hosts bring new parasites that have detrimental effects on native hosts) predict that the local host will be most likely to experience a disadvantage. However, few studies evaluate the occurrence of interspecific parasite transfer by performing wide-scale geographic sampling of pathogen lineages, both within and far from host contact zones. In this study, we investigate how haemosporidian (avian malaria) prevalence and lineage diversity vary in two, closely related species of passerine birds; the pied flycatcher Ficedula hypoleuca and the collared flycatcher F. albicollis in both allopatry and sympatry. We find that host species is generally a better predictor of parasite diversity than location, but both prevalence and diversity of parasites vary widely among populations of the same bird species. We also find a limited and unidirectional transfer of parasites from pied flycatchers to collared flycatchers in a recent contact zone. This study therefore rejects both the Enemy Release Hypothesis and the Novel Weapon Hypothesis and highlights the complexity and importance of studying host-parasite relationships in an era of global climate change and species range shifts.
    https://doi.org/10.1002/ece3.4677
  • Frontiers in Ecology and the Environment
    10-2018

    Artificial light at night as a driver of evolution across urban-rural landscapes

    Gareth R. Hopkins, Kevin J. Gaston, Marcel E. Visser, Mark A. Elgar, Therésa M. Jones
    Light is fundamental to biological systems, affecting the daily rhythms of bacteria, plants, and animals. Artificial light at night (ALAN), a ubiquitous feature of urbanization, interferes with these rhythms and has the potential to exert strong selection pressures on organisms living in urban environments. ALAN also fragments landscapes, altering the movement of animals into and out of artificially lit habitats. Although research has documented phenotypic and genetic differentiation between urban and rural organisms, ALAN has rarely been considered as a driver of evolution. We argue that the fundamental importance of light to biological systems, and the capacity for ALAN to influence multiple processes contributing to evolution, makes this an important driver of evolutionary change, one with the potential to explain broad patterns of population differentiation across urban-rural landscapes. Integrating ALAN's evolutionary potential into urban ecology is a targeted and powerful approach to understanding the capacity for life to adapt to an increasingly urbanized world.
    https://doi.org/10.1002/fee.1828
  • PLoS One
    19-09-2018

    Wild great and blue tits do not avoid chemical cues of predators when selecting cavities for roosting

    Luisa Amo de Paz, G. Tomas Gutierrez, Irene Saavedra, Marcel E. Visser
    Small birds use cavities for roosting to decrease the thermoregulatory costs during the winter nights. The ability of birds to detect and escape from an approaching predator is impaired during roosting and thus the selection of such cavities should take into account the risk that a predator will find the cavity. Previous evidence suggested that birds in captivity are able to detect predator scent and avoid roosting in nest-boxes containing such predator chemical cues. Here, we tested whether birds also show this avoidance response under natural conditions. We performed three studies in three populations of blue and great tits. We added predator scent, a pungency scent or an odourless control to nest-boxes and compared the use of these nest-boxes for roosting. We found no differences between the scent treatments in the use of nest-boxes. Therefore, chemical cues indicating the potential presence of a predator are not enough for birds to avoid roosting in nest-boxes under natural conditions.
    https://doi.org/10.1371/journal.pone.0203269
  • Journal of Experimental Zoology Part A: Ecological and Integrative Physiology
    29-07-2018

    Dose-response effects of light at night on the reproductive physiology of great tits (Parus major): Integrating morphological analyses with candidate gene expression

    Davide Dominoni, Maaike de Jong, Michelle Bellingham, Peter O’Shaughnessy, Kees van Oers, Jane Robinson, Bethany Smith, Marcel E. Visser, Barbara Helm
    Abstract Artificial light at night (ALAN) is increasingly recognized as a potential threat to wildlife and ecosystem health. Among the ecological effects of ALAN, changes in reproductive timing are frequently reported, but the mechanisms underlying this relationship are still poorly understood. Here, we experimentally investigated these mechanisms by assessing dose-dependent photoperiodic responses to ALAN in the great tit (Parus major). We individually exposed photosensitive male birds to one of three nocturnal light levels (0.5, 1.5, and 5 lux), or to a dark control. Subsequent histological and molecular analyses on their testes indicated a dose-dependent reproductive response to ALAN. Specifically, different stages of gonadal growth were activated after exposure to different levels of light at night. mRNA transcript levels of genes linked to the development of germ cells (stra8 and spo11) were increased under 0.5 lux compared to the dark control. The 0.5 and 1.5 lux groups showed slight increases in testis size and transcript levels associated with steroid synthesis (lhr and hsd3b1) and spermatogenesis (fshr, wt1, sox9, and cldn11), although spermatogenesis was not detected in histological analysis. In contrast, all birds under 5 lux had 10 to 30 times larger testes than birds in all other groups, with a parallel strong increase in mRNA transcript levels and clear signs of spermatogenesis. Across treatments, the volume of the testes was generally a good predictor of testicular transcript levels. Overall, our findings indicate that even small changes in nocturnal light intensity can increase, or decrease, effects on the reproductive physiology of wild organisms.
    https://doi.org/10.1002/jez.2214
  • Journal of Experimental Zoology Part A: Ecological and Integrative Physiology
    27-06-2018

    Effects of experimental light at night on extra-pair paternity in a songbird

    Maaike de Jong, K.P. Lamers, Mark Eugster, Jenny Ouyang, Arnaud Da Silva, A.C. Mateman, Roy H. A. van Grunsven, Marcel E. Visser, Kamiel Spoelstra
    Abstract Light pollution is increasing worldwide and significantly affects animal behavior. In birds, these effects include advancement of morning activity and onset of dawn song, which may affect extra-pair paternity. Advanced dawn song of males may stimulate females to engage in extra-pair copulations, and the earlier activity onset may affect the males? mate guarding behavior. Earlier work showed an effect of light at night on extra-pair behavior, but this was in an area with other anthropogenic disturbances. Here, we present a two-year experimental study on effects of light at night on extra-pair paternity of great tits (Parus major). Previously dark natural areas were illuminated with white, red, and green LED lamps and compared to a dark control. In 2014, the proportion of extra-pair young in broods increased with distance to the red and white lamps (i.e., at lower light intensities), but decreased with distance to the poles in the dark control. In 2013, we found no effects on the proportion of extra-pair young. The total number of offspring sired by a male was unaffected by artificial light at night in both years, suggesting that potential changes in female fidelity in pairs breeding close to white and red light did not translate into fitness benefits for the males of these pairs. Artificial light at night might disrupt the natural patterns of extra-pair paternity, possibly negates potential benefits of extra-pair copulations and thus could alter sexual selection processes in wild birds.
    https://doi.org/10.1002/jez.2193
  • Global Change Biology
    06-04-2018

    Phenological sensitivity to climate change is higher in resident than in migrant bird populations among European cavity breeders

    Jelmer M. Samplonius, Lenka Bartošová, Malcolm D. Burgess, Andrey Bushuev, Tapio Eeva, Elena V. Ivankina, Anvar B. Kerimov, Indrikis Krams, Toni Laaksonen, Marko Mägi, Raivo Mänd, Jaime Potti, János Török, Miroslav Trnka, Marcel E. Visser, Herwig Zang, Christiaan Both
    Abstract Many organisms adjust their reproductive phenology in response to climate change, but phenological sensitivity to temperature may vary between species. For example, resident and migratory birds have vastly different annual cycles, which can cause differential temperature sensitivity at the breeding grounds, and may affect competitive dynamics. Currently, however, adjustment to climate change in resident and migratory birds have been studied separately or at relatively small geographical scales with varying time series durations and methodologies. Here, we studied differential effects of temperature on resident and migratory birds using the mean egg laying initiation dates from 10 European nest box schemes between 1991 and 2015 that had data on at least one resident tit species and at least one migratory flycatcher species. We found that both tits and flycatchers advanced laying in response to spring warming, but resident tit populations advanced more strongly in relation to temperature increases than migratory flycatchers. These different temperature responses have already led to a divergence in laying dates between tits and flycatchers of on average 0.94 days per decade over the current study period. Interestingly, this divergence was stronger at lower latitudes where the interval between tit and flycatcher phenology is smaller and winter conditions can be considered more favorable for resident birds. This could indicate that phenological adjustment to climate change by flycatchers is increasingly hampered by competition with resident species. Indeed, we found that tit laying date had an additional effect on flycatcher laying date after controlling for temperature, and this effect was strongest in areas with the shortest interval between both species groups. Combined, our results suggest that the differential effect of climate change on species groups with overlapping breeding ecology affects the phenological interval between them, potentially affecting interspecific interactions.
    https://doi.org/10.1111/gcb.14160
  • Proceedings of the Royal Society B-Biological Sciences
    28-03-2018

    Artificial light at night shifts daily activity patterns but not the internal clock in the great tit (Parus major)

    Kamiel Spoelstra, Irene C. Verhagen, Davy Meijer, Marcel E. Visser
    Artificial light at night has shown a dramatic increase over the last decades and continues to increase. Light at night can have strong effects on the behaviour and physiology of species, which includes changes in the daily timing of activity; a clear example is the advance in dawn song onset in songbirds by low levels of light at night. Although such effects are often referred to as changes in circadian timing, i.e. changes to the internal clock, two alternative mechanisms are possible. First, light at night can change the timing of clock controlled activity, without any change to the clock itself; e.g. by a change in the phase relation between the circadian clock and expression of activity. Second, changes in daily activity can be a direct response to light (‘masking’), without any involvement of the circadian system. Here, we studied whether the advance in onset of activity by dim light at night in great tits (Parus major) is indeed attributable to a phase shift of the internal clock. We entrained birds to a normal light/dark (LD) cycle with bright light during daytime and darkness at night, and to a comparable (LDim) schedule with dim light at night. The dim light at night strongly advanced the onset of activity of the birds. After at least six days in LD or LDim, we kept birds in constant darkness (DD) by leaving off all lights so birds would revert to their endogenous, circadian system controlled timing of activity. We found that the timing of onset in DD was not dependent on whether the birds were kept at LD or LDim before the measurement. Thus, the advance of activity under light at night is caused by a direct effect of light rather than a phase shift of the internal clock. This demonstrates that birds are capable of changing their daily activity to low levels of light at night directly, without the need to alter their internal clock.
    https://doi.org/10.1098/rspb.2017.2751
  • BMC Genomics
    2018

    CNVs are associated with genomic architecture in a songbird

    Vinicius Henrique da Silva, Veronika Laine, Mirte Bosse, Kees van Oers, Bert W. Dibbits, Marcel E. Visser, Richard P. M. A. Crooijmans, Martien A.M. Groenen
    Understanding variation in genome structure is essential to understand phenotypic differences within populations and the evolutionary history of species. A promising form of this structural variation is copy number variation (CNV). CNVs can be generated by different recombination mechanisms, such as non-allelic homologous recombination, that rely on specific characteristics of the genome architecture. These structural variants can therefore be more abundant at particular genes ultimately leading to variation in phenotypes under selection. Detailed characterization of CNVs therefore can reveal evolutionary footprints of selection and provide insight in their contribution to phenotypic variation in wild populations.
    https://doi.org/10.1186/s12864-018-4577-1
  • American Naturalist
    2018

    Maternal effects in a wild songbird are environmentally plastic but only marginally alter the rate of adaptation

    Jip Ramakers, Marleen Cobben, Piter Bijma, T. E. Reed, Marcel E. Visser, Phillip Gienapp
    Despite ample evidence for the presence of maternal effects (MEs) in a variety of traits and strong theoretical indications for their evolutionary consequences, empirical evidence to what extent MEs can influence evolutionary responses to selection remains ambiguous. We tested the degree to which MEs can alter the rate of adaptation of a key life-history trait, clutch size, using an individual-based model approach parameterized with experimental data from a long-term study of great tits (Parus major). We modeled two types of MEs: (i) an environmentally plastic ME, in which the relationship between maternal and offspring clutch size depended on the maternal environment via offspring condition, and (ii) a fixed ME, in which this relationship was constant. Although both types of ME affected the rate of adaptation following an abrupt environmental shift, the overall effects were small. We conclude that evolutionary consequences of MEs are modest at best in our study system, at least for the trait and the particular type of ME we considered here. A closer link between theoretical and empirical work on MEs would hence be useful to obtain accurate predictions about the evolutionary consequences of MEs more generally.
    https://doi.org/10.1086/696847
  • Journal of Experimental Zoology Part A: Ecological Genetics and Physiology
    2018

    No effect of artificial light of different colors on commuting Daubenton's bats (Myotis daubentonii) in a choice experiment

    Progressive illumination at night poses an increasing threat to species worldwide. Light at night is particularly problematic for bats as most species are nocturnal and often cross relatively large distances when commuting between roosts and foraging grounds. Earlier studies have shown that illumination of linear structures in the landscape disturbs commuting bats, and that the response of bats to light may strongly depend on the light spectrum. Here, we studied the impact of white, green, and red light on commuting Daubenton's bats (Myotis daubentonii). We used a unique location where commuting bats cross a road by flying through two identical, parallel culverts underneath. We illuminated the culverts with white, red, and green light,with an intensity of 5 lux at the water surface. Bats had to choose between the two culverts, each with a different lighting condition every night. We presented all paired combinations of white, green, and red light and dark control in a factorial design. Contrary to our expectations, the number of bat passes through a culvert was unaffected by the presence of light. Furthermore, bats did not show any preference for light color. These results show that the response of commuting Daubenton's bats to different colors of light at night with a realistic intensity may be limited when passing through culverts.
    https://doi.org/10.1002/jez.2178
  • Global Change Biology
    2018

    Climate change leads to differential shifts in the timing of annual cycle stages in a migratory bird

    Barbara Tomotani, Henk P. van der Jeugd, Phillip Gienapp, Iván De la Hera, J. Pilzecker, Corry Teichmann, Marcel E. Visser
    Shifts in reproductive phenology due to climate change have been well documented in many species but how, within the same species, other annual cycle stages (e.g., moult, migration) shift relative to the timing of breeding has rarely been studied. When stages shift at different rates, the interval between stages may change resulting in overlaps, and as each stage is energetically demanding, these overlaps may have negative fitness consequences. We used long-term data of a population of European pied flycatchers (Ficedula hypoleuca) to investigate phenological shifts in three annual cycle stages: spring migration (arrival dates), breeding (egg-laying and hatching dates) and the onset of post-breeding moult. We found different advancements in the timing of breeding compared to moult (moult advances faster) and no advancement in arrival dates. To understand these differential shifts, we explored which temperatures best explain the year-to-year variation in the timing of these stages, and show that they respond differently to temperature increases in the Netherlands, causing the intervals between arrival and breeding and between breeding and moult to decrease. Next, we tested the fitness consequences of these shortened intervals. We found no effect on clutch size, but the probability of a fledged chick to recruit increased with a shorter arrival-breeding interval (earlier breeding). Finally, mark-recapture analyses did not detect an effect of shortened intervals on adult survival. Our results suggest that the advancement of breeding allows more time for fledgling development, increasing their probability to recruit. This may incur costs to other parts of the annual cycle but, despite the shorter intervals, there was no effect on adult survival. Our results show that to fully understand the consequences of climate change, it is necessary to look carefully at different annual cycle stages, especially for organisms with complex cycles, such as migratory birds.
    https://doi.org/10.1111/gcb.14006
  • Ardea
    2018

    Timing of avian breeding in an urbanized world

    Maaike de Jong, L. Van den Eertwegh, R. Beskers, Peter De Vries, Kamiel Spoelstra, Marcel E. Visser
    A large part of the world is urbanized, and the process of urbanization is ongoing.
    Species differ in the extent to which they are impacted by urbanization, depending
    on adaption capacity, and on the fitness consequences when adaptation lags
    behind. One prominent effect of urbanization is the dramatic change of the nighttime
    environment: in urban areas nights are no longer dark. Here, we studied the
    impact of urbanization on the timing of breeding, which is a key life-history trait.
    We used six years of data from ten common bird species, breeding in nest boxes
    throughout the Netherlands. We took the intensity of artificial light in the form of
    zenithal sky brightness and light emission, as a proxy for urbanization. We found
    a correlation between light levels and seasonal timing in three of the ten species
    (great tit, blue tit and pied flycatcher), but these relationships differed between
    years. The effect of urbanization on seasonal timing is at best weak in our study
    which was however mainly based on areas with relatively low light levels. There is
    a clear lack of data for breeding birds in more urbanized environments, an ever
    expanding habitat for an increasing number of species worldwide.
    https://doi.org/10.5253/arde.v106i1.a4
  • Functional Ecology
    2018

    Photoperiodic cues regulate phenological carry-over effects in an herbivorous insect

    Lucia Salis, E. van den Hoorn, Domien G. M. Beersma, Roelof A Hut, Marcel E. Visser
    To maximise their fitness, organisms need to synchronise their phenology with the seasonal variation in environmental conditions. Most phenological traits are affected by environmental abiotic cues such as photoperiod, temperature and rainfall. When individuals with complex life cycles fail to match one of the stages with the favourable environment, the negative conditions experienced may lead to carry-over effects and, thus, influence fitness in subsequent stages.
    In the winter moth, an herbivorous insect with an annual life cycle, timing of egg-hatching in spring is strongly influenced by temperature and varies from year to year. To investigate whether the phenological variation in egg-hatching date affects subsequent stages, we analysed data on egg-hatching date and adult catching date (considered here to be a proxy for adult eclosion date) from our long-term study (1994–2014). Furthermore, we experimentally manipulated the photoperiod experienced by newly hatched larvae and recorded the phenology of their subsequent life cycle stages.
    In the long-term field study, we found that the timing of winter moth egg-hatching in spring varied strongly from year to year. Interestingly, however, the timing of adult eclosion date in winter showed little inter-annual variation. In line with these findings, our experimental data showed that the winter moth shortened the duration of their pupal development when they experienced a late spring photoperiod as a larva, and prolonged pupal development when experiencing early spring photoperiod. The effects of the larval photoperiodic treatments persisted during egg development in the following generation.
    The results show that a phenological shift that occurs during an early life stage is partially compensated during subsequent stages and suggest that the mechanism underlying this compensation is mediated by photoperiod. Winter moths regulated their phenology in such a way that the variation in the egg-hatching stage was not carried over to the next life cycle stages. This has strong effects on fitness as it (1) ensures the synchronisation of adult eclosion during the mating period and (2) is likely to reduce potentially negative fitness consequences of phenological mismatches in egg-hatching in the following generation. Overall, these findings stress the importance of understanding phenological carry-over effects to forecast the impact of global change in species with complex life cycles.
    https://doi.org/10.1111/1365-2435.12953
  • Functional Ecology
    2018

    Simulated moult reduces flight performance but overlap with breeding does not affect breeding success in a long-distance migrant

    Barbara Tomotani, Florian T. Muijres, Julia Koelman, Stefania Casagrande, Marcel E. Visser
    * Long-distance migrants are time-constrained as they need to incorporate many annual cycle stages within a year. Migratory passerines moult in the short interval between breeding and migration. To widen this interval, moult may start while still breeding, but this results in flying with moulting wings when food provisioning. * We experimentally simulated wing gaps in breeding male pied flycatchers by plucking two primary feathers from both wings. We quantified the nest visitations of both parents, proportion of high-quality food brought to the nestlings and adults and nestlings condition. Differences in oxidative damage caused by a possible reduction in flight efficiency were measured in amounts of ROMs and OXY in the blood. We also measured how flight performance was affected with recordings of the male`s escape flight using high-speed cameras. Finally, we collected data on adult survival, clutch size and laying date in the following year. * “Plucked” males travelled a 5% shorter distance per wingbeat, showing that our treatment reduced flight performance. In line with this, “plucked” males visited their nests less often. Females of “plucked” males, however, visited the nest more often than controls, and fully compensated their partner's reduced visitation rate. As a result, there were no differences between treatments in food quality brought to the nest, adult or chick mass or number of successfully fledged chicks. Males did not differ in their oxidative damage or local survival to the following year. In contrast, females paired with plucked males tended to return less often to breed in the next year in comparison to controls, but this difference was not significant. For the birds that did return, there were no effects on breeding. * Our results reveal that wing gaps in male pied flycatchers reduce their flight performance, but when it occurs during breeding they prioritise their future reproduction by reducing parental care. As a result, there is no apparent detriment to their condition during breeding. Because non-moulting females are able to compensate their partner's reduced care, there is also no immediate cost to the offspring, but females may pay the cost suffering from a reduced survival. A plain language summary is available for this article.
    https://doi.org/10.1111/1365-2435.12974
  • Molecular Ecology Resources
    2018

    A high density SNP chip for genotyping great tit (Parus major) populations and its application to studying the genetic architecture of exploration behaviour

    Jung-Mi Kim, A.W. Santure, Henry J Barton, J.L. Quinn, Eleanor F. Cole, Marcel E. Visser, Ben C. Sheldon, M.A.M. Groenen, Kees van Oers, Jon Slate
    High density SNP microarrays (‘SNP chips’) are a rapid, accurate and efficient method for genotyping several hundred thousand polymorphisms in large numbers of individuals. While SNP chips are routinely used in human genetics and in animal and plant breeding, they are less widely used in evolutionary and ecological research. In this paper we describe the development and application of a high density Affymetrix Axiom chip with around 500 000 SNPs, designed to perform genomics studies of great tit (Parus major) populations. We demonstrate that the per‐SNP genotype error rate is well below 1% and that the chip can also be used to identify structural or copy number variation (CNVs). The chip is used to explore the genetic architecture of exploration behaviour (EB), a personality trait that has been widely studied in great tits and other species. No SNPs reached genome‐wide significance, including at DRD4, a candidate gene. However, EB is heritable and appears to have a polygenic architecture. Researchers developing similar SNP chips may note: (i) SNPs previously typed on alternative platforms are more likely to be converted to working assays, (ii) detecting SNPs by more than one pipeline, and in independent datasets, ensures a high proportion of working assays, (iii) allele frequency ascertainment bias is minimised by performing SNP discovery in individuals from multiple populations and (iv) samples with the lowest call rates tend to also have the greatest genotyping error rates.
    https://doi.org/10.1111/1755-0998.12778
  • Nature Ecology and Evolution
    2018

    Navigating the unfolding open data landscape in ecology and evolution

    Antica Culina, Miriam Baglioni, Tom Crowther, Marcel E. Visser, Saskia Woutersen, P. Manghi
    Open access to data is revolutionizing the sciences. To allow ecologists and evolutionary biologists to confidently find and use the existing data, we provide an overview of the landscape of online data infrastructures, and highlight the key points to consider when using open data. We introduce an online collaborative platform to keep a community-driven, updated list of the best sources that enable search for data in one interface. In doing so, our aim is to lower the barrier to accessing open data, and encourage its use by researchers hoping to increase the scope, reliability and value of their findings.
    https://doi.org/10.1038/s41559-017-0458-2
  • New Phytologist
    2018

    Covariation and phenotypic integration in chemical communication displays: biosynthetic constraints and eco-evolutionary implications

    Robert R. Junker, Jonas Kuppler, Luisa Amo de Paz, James D. Blande, Renee M. Borges, Nicole M. van Dam, Marcel Dicke, Stefan Dötterl, Bodil K. Ehlers, Florian Etl, Jonathan Gershenzon, Robert Glinwood, Rieta Gols, Astrid T. Groot, Martin Heil, Mathias Hoffmeister, Jarmo K. Holopainen, Stefan Jarau, Lena John, André Kessler, Jette T. Knudsen, Christian Kost, Anne-Amélie C. Larue-Kontic, Sara Diana Leonhardt, Dani Lucas-Barbosa, Cassie J. Majetic, Florian Menzel, Amy L. Parachnowitsch, Rémy S. Pasquet, Erik H. Poelman, Robert A. Raguso, Joachim Ruther, FLORIAN P. SCHIESTL, Thomas Schmitt, Dorothea Tholl, Sybille B. Unsicker, Niels O. Verhulst, Marcel E. Visser, Berhane T. Weldegergis, Tobias G. Köllner
    •Chemical communication is ubiquitous. The identification of conserved structural elements in visual and acoustic communication is well established, but comparable information on chemical communication displays (CCDs) is lacking.
    •We assessed the phenotypic integration of CCDs in a meta-analysis to characterize patterns of covariation in CCDs and identified functional or biosynthetically constrained modules.
    •Poorly integrated plant CCDs (i.e. low covariation between scent compounds) support the notion that plants often utilize one or few key compounds to repel antagonists or to attract pollinators and enemies of herbivores. Animal CCDs (mostly insect pheromones) were usually more integrated than those of plants (i.e. stronger covariation), suggesting that animals communicate via fixed proportions among compounds. Both plant and animal CCDs were composed of modules, which are groups of strongly covarying compounds. Biosynthetic similarity of compounds revealed biosynthetic constraints in the covariation patterns of plant CCDs.
    •We provide a novel perspective on chemical communication and a basis for future investigations on structural properties of CCDs. This will facilitate identifying modules and biosynthetic constraints that may affect the outcome of selection and thus provide a predictive framework for evolutionary trajectories of CCDs in plants and animals.
    https://doi.org/10.1111/nph.14505
  • Nature Ecology and Evolution
    2018

    Environmental coupling of heritability and selection is rare and of minor evolutionary significance in wild populations

    Jip Ramakers, Antica Culina, Marcel E. Visser, Phillip Gienapp
    Predicting the rate of adaptation to environmental change in wild populations is important for understanding evolutionary
    change. However, predictions may be unreliable if the two key variables affecting the rate of evolutionary change—heritability
    and selection—are both affected by the same environmental variable. To determine how general such an environmentally
    induced coupling of heritability and selection is, and how this may influence the rate of adaptation, we made use of freely accessible,
    open data on pedigreed wild populations to answer this question at the broadest possible scale. Using 16 populations from 10 vertebrate species, which provided data on 50 traits (relating to body mass, morphology, physiology, behaviour and
    life history), we found evidence for an environmentally induced relationship between heritability and selection in only 6 cases, with weak evidence that this resulted in an increase or decrease in the expected selection response. We conclude that such a coupling of heritability and selection is unlikely to strongly affect evolutionary change, even though both heritability and selection are commonly postulated to be dependent on the environment.
    https://doi.org/10.1038/s41559-018-0577-4
  • Nature Ecology and Evolution
    2018

    How to do meta-analysis of open datasets

    Antica Culina, Tom Crowther, Jip Ramakers, Phillip Gienapp, Marcel E. Visser
    The amount of open data in ecology and evolution is increasing rapidly, yet this resource remains underused. Here, we introduce a new framework and case study for conducting meta-analyses of open datasets, and discuss its benefits and current limitations.
    https://doi.org/10.1038/s41559-018-0579-2
  • Genome Biology and Evolution
    01-11-2017

    Determinants of the Efficacy of Natural Selection on Coding and Noncoding Variability in Two Passerine Species

    Pádraic Corcoran, Toni I. Gossmann, Henry J Barton, Jon Slate, Kai Zeng, Veronika Laine, Kees van Oers, Koen Verhoeven, Marcel E. Visser
    Population genetic theory predicts that selection should be more effective when the effective population size (Ne) is larger, and that the efficacy of selection should correlate positively with recombination rate. Here, we analyzed the genomes of ten great tits and ten zebra finches. Nucleotide diversity at 4-fold degenerate sites indicates that zebra finches have a 2.83-fold larger Ne. We obtained clear evidence that purifying selection is more effective in zebra finches. The proportion of substitutions at 0-fold degenerate sites fixed by positive selection (α) is high in both species (great tit 48%; zebra finch 64%) and is significantly higher in zebra finches. When α was estimated on GC-conservative changes (i.e., between A and T and between G and C), the estimates reduced in both species (great tit 22%; zebra finch 53%). A theoretical model presented herein suggests that failing to control for the effects of GC-biased gene conversion (gBGC) is potentially a contributor to the overestimation of α, and that this effect cannot be alleviated by first fitting a demographic model to neutral variants. We present the first estimates in birds for α in the untranslated regions, and found evidence for substantial adaptive changes. Finally, although purifying selection is stronger in high-recombination regions, we obtained mixed evidence for α increasing with recombination rate, especially after accounting for gBGC. These results highlight that it is important to consider the potential confounding effects of gBGC when quantifying selection and that our understanding of what determines the efficacy of selection is incomplete.
    https://doi.org/10.1093/gbe/evx213
  • Science
    20-10-2017

    Recent natural selection causes adaptive evolution of an avian polygenic trait

    Mirte Bosse, Lewis G. Spurgin, Veronika Laine, Ella F. Cole, Josh A. Firth, Phillip Gienapp, Andrew G. Gosler, Keith McMahon, Jocelyn Poissant, Irene C. Verhagen, Martien A.M. Groenen, Kees van Oers, Ben C. Sheldon, Marcel E. Visser, Jon Slate
    Many studies have found evidence of rapid evolution in response to environmental change. In most cases, there has been some suggestion of which traits might be most responsive ahead of time. Bosse et al. turn this approach on its head by using genomic regions with a signature of selection to identify traits that are changing. In great tits (Parus major) in the United Kingdom, genomic regions showing selection invariably contained genes associated with bill growth. Indeed, U.K. birds not only have longer bills, but these longer bills are associated with increased fitness. These changes likely reflect an increase in domestic garden bird feeders over the past several decades.Science, this issue p. 365We used extensive data from a long-term study of great tits (Parus major) in the United Kingdom and Netherlands to better understand how genetic signatures of selection translate into variation in fitness and phenotypes. We found that genomic regions under differential selection contained candidate genes for bill morphology and used genetic architecture analyses to confirm that these genes, especially the collagen gene COL4A5, explained variation in bill length. COL4A5 variation was associated with reproductive success, which, combined with spatiotemporal patterns of bill length, suggested ongoing selection for longer bills in the United Kingdom. Last, bill length and COL4A5 variation were associated with usage of feeders, suggesting that longer bills may have evolved in the United Kingdom as a response to supplementary feeding.
    https://doi.org/10.1126/science.aal3298
  • Integrative and Comparative Biology
    16-10-2017

    Understanding Evolutionary Impacts of Seasonality: An Introduction to the Symposium

    Caroline M. Williams, Gregory J. Ragland, Gustavo Betini, Lauren B. Buckley, Zachary A. Cheviron, Kathleen Donohue, Joe Hereford, Murray M. Humphries, Simeon Lisovski, Katie E. Marshall, Paul S. Schmidt, Kimberly S. Sheldon, Øystein Varpe, Marcel E. Visser
    Seasonality is a critically important aspect of environmental variability, and strongly shapes all aspects of life for organisms living in highly seasonal environments. Seasonality has played a key role in generating biodiversity, and has driven the evolution of extreme physiological adaptations and behaviors such as migration and hibernation. Fluctuating selection pressures on survival and fecundity between summer and winter provide a complex selective landscape, which can be met by a combination of three outcomes of adaptive evolution: genetic polymorphism, phenotypic plasticity, and bet-hedging. Here, we have identified four important research questions with the goal of advancing our understanding of evolutionary impacts of seasonality. First, we ask how characteristics of environments and species will determine which adaptive response occurs. Relevant characteristics include costs and limits of plasticity, predictability, and reliability of cues, and grain of environmental variation relative to generation time. A second important question is how phenological shifts will amplify or ameliorate selection on physiological hardiness. Shifts in phenology can preserve the thermal niche despite shifts in climate, but may fail to completely conserve the niche or may even expose life stages to conditions that cause mortality. Considering distinct environmental sensitivities of life history stages will be key to refining models that forecast susceptibility to climate change. Third, we must identify critical physiological phenotypes that underlie seasonal adaptation and work toward understanding the genetic architectures of these responses. These architectures are key for predicting evolutionary responses. Pleiotropic genes that regulate multiple responses to changing seasons may facilitate coordination among functionally related traits, or conversely may constrain the expression of optimal phenotypes. Finally, we must advance our understanding of how changes in seasonal fluctuations are impacting ecological interaction networks. We should move beyond simple dyadic interactions, such as predator prey dynamics, and understand how these interactions scale up to affect ecological interaction networks. As global climate change alters many aspects of seasonal variability, including extreme events and changes in mean conditions, organisms must respond appropriately or go extinct. The outcome of adaptation to seasonality will determine responses to climate change.
    https://doi.org/10.1093/icb/icx122
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    09-10-2017

    Chronobiology of interspecific interactions in a changing world

    Noga Kronfeld-Schor, Marcel E. Visser, Lucia Salis, J.A. Van Gils
    Animals should time activities, such as foraging, migration and reproduction, as well as seasonal physiological adaptation, in a way that maximizes fitness. The fitness outcome of such activities depends largely on their interspecific interactions; the temporal overlap with other species determines when they should be active in order to maximize their encounters with food and to minimize their encounters with predators, competitors and parasites. To cope with the constantly changing, but predictable structure of the environment, organisms have evolved internal biological clocks, which are synchronized mainly by light, the most predictable and reliable environmental cue (but which can be masked by other variables), which enable them to anticipate and prepare for predicted changes in the timing of the species they interact with, on top of responding to them directly. Here, we review examples where the internal timing system is used to predict interspecific interactions, and how these interactions affect the internal timing system and activity patterns. We then ask how plastic these mechanisms are, how this plasticity differs between and within species and how this variability in plasticity affects interspecific interactions in a changing world, in which light, the major synchronizer of the biological clock, is no longer a reliable cue owing to the rapidly changing climate, the use of artificial light and urbanization.This article is part of the themed issue ‘Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals’.
    https://doi.org/10.1098/rstb.2016.0248
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    09-10-2017

    Two sides of a coin: ecological and chronobiological perspectives of timing in the wild

    Barbara Helm, Marcel E. Visser, William Schwartz, Noga Kronfeld-Schor, Menno Gerkema, Theunis Piersma, Guy Bloch
    Most processes within organisms, and most interactions between organisms and their environment, have distinct time profiles. The temporal coordination of such processes is crucial across levels of biological organization, but disciplines differ widely in their approaches to study timing. Such differences are accentuated between ecologists, who are centrally concerned with a holistic view of an organism in relation to its external environment, and chronobiologists, who emphasize internal timekeeping within an organism and the mechanisms of its adjustment to the environment. We argue that ecological and chronobiological perspectives are complementary, and that studies at the intersection will enable both fields to jointly overcome obstacles that currently hinder progress. However, to achieve this integration, we first have to cross some conceptual barriers, clarifying prohibitively inaccessible terminologies. We critically assess main assumptions and concepts in either field, as well as their common interests. Both approaches intersect in their need to understand the extent and regulation of temporal plasticity, and in the concept of ‘chronotype’, i.e. the characteristic temporal properties of individuals which are the targets of natural and sexual selection. We then highlight promising developments, point out open questions, acknowledge difficulties and propose directions for further integration of ecological and chronobiological perspectives through Wild Clock research.This article is part of the themed issue ‘Wild Clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals’.
    https://doi.org/10.1098/rstb.2016.0246
  • Journal of Biological Rhythms
    26-07-2017

    Early Birds by Light at Night: Effects of Light Color and Intensity on Daily Activity Patterns in Blue Tits

    Maaike de Jong, Samuel P. Caro, Phillip Gienapp, Kamiel Spoelstra, Marcel E. Visser
    Artificial light at night disturbs the daily rhythms of many organisms. To what extent this disturbance depends on the intensity and spectral composition of light remain obscure. Here, we measured daily activity patterns of captive blue tits (Cyanistes caeruleus) exposed to similar intensities of green, red, or white light at night. Birds advanced their onset of activity in the morning under all light colors but more under red and white light than under green light. Offset of activity was slightly delayed in all light colors. The total activity over a 24-h period did not change but birds moved a part of their daily activity into the night. Since the effect of red and white lights are comparable, we tested the influence of light intensity in a follow-up experiment, where we compared the activity of the birds under different intensities of green and white light only. While in the higher range of intensities, the effects of white and green light were comparable; at lower intensities, green light had a less disturbing effect as compared with white light on daily rhythms in blue tits. Our results show that the extent of this disturbance can be mitigated by modulating the spectral characteristics and intensity of outdoor lighting, which is now feasible through the use of LED lighting.
    https://doi.org/10.1177/0748730417719168
  • Proceedings of the Royal Society B-Biological Sciences
    06-2017

    Response of bats to light with different spectra: light-shy and agile bat presence is affected by white and green, but not red light

    Kamiel Spoelstra, Roy H. A. van Grunsven, Jip Ramakers, Kim Ferguson, Thomas Raap, Maurice Donners, Elmar M. Veenendaal, Marcel E. Visser
    Artificial light at night has shown a remarkable increase over the past decades. Effects are reported for many species groups, and include changes in presence, behaviour, physiology and life-history traits. Among these, bats are strongly affected, and how bat species react to light is likely to vary with light colour. Different spectra may therefore be applied to reduce negative impacts. We used a unique set-up of eight field sites to study the response of bats to three different experimental light spectra in an otherwise dark and undisturbed natural habitat. We measured activity of three bat species groups around transects with light posts emitting white, green and red light with an intensity commonly used to illuminate countryside roads. The results reveal a strong and spectrum-dependent response for the slow-flying Myotis and Plecotus and more agile Pipistrellus species, but not for Nyctalus and Eptesicus species. Plecotus and Myotis species avoided white and green light, but were equally abundant in red light and darkness. The agile, opportunistically feeding Pipistrellus species were significantly more abundant around white and green light, most likely because of accumulation of insects, but equally abundant in red illuminated transects compared to dark control. Forest-dwelling Myotis and Plecotus species and more synanthropic Pipistrellus species are thus least disturbed by red light. Hence, in order to limit the negative impact of light at night on bats, white and green light should be avoided in or close to natural habitat, but red lights may be used if illumination is needed.
    https://doi.org/10.1098/rspb.2017.0075
  • Frontiers in Ecology and Evolution
    30-05-2017

    Artificial Light at Night Reduces Daily Energy Expenditure in Breeding Great Tits (Parus major)

    Anouk Welbers, Natalie van Dis, Annemieke Kolvoort, Jenny Ouyang, Marcel E. Visser, Kamiel Spoelstra, Davide Dominoni
    The ecological impact of artificial light at night (ALAN) is an increasingly recognized process that accompanies expanding urbanization. Yet, we have limited knowledge on the impact of ALAN on wild species, and on the potential to mitigate any negative effects by using different light sources and colors. In birds, effects of ALAN on activity levels are reported for several species and, hence, their daily energy expenditure (DEE) may be affected. DEE is a potent mediator of life-history trade-offs and fitness and thus an important aspect to consider when examining the potential long-term ecological effects of ALAN. Previous work has suggested that birds exposed to ALAN show higher levels of provisioning and nocturnal activity, suggesting that white ALAN increases DEE. Other factors regulating DEE, such as provisioning behavior and food availability, might also respond to ALAN and thus indirectly affect DEE. We tested the hypothesis that ALAN increases DEE using an experimental setup where four previously unlit transects were illuminated with either white, green, or red LED light, or left dark as a control treatment. This setup was replicated in eight locations across the Netherlands. We measured DEE of our focal species, the great tit (Parus major), using a novel doubly labeled water technique that uses breath rather than blood samples. Contrary to our expectations, birds feeding their offspring under white and green ALAN showed lower DEE compared to birds in the control dark treatment. Differences in chick provisioning activity did not explain this result, as neither visit rates nor daily activity timing was affected by light treatment. However, food availability under white and green light was much higher compared to red light and the dark control. This difference strongly suggests that the lower DEE under white and green ALAN sites is a consequence of higher food availability in these treatments. This result shows that there can be positive, indirect effects of ALAN for breeding song birds which may balance against the negative direct effects shown in previous studies.
    https://doi.org/10.3389/fevo.2017.00055
  • Journal of Avian Biology
    15-03-2017

    Early arrival is not associated with more extra-pair fertilizations in a long-distance migratory bird

    Barbara Tomotani, Ezra Caglar, Iván De la Hera, A.C. Mateman, Marcel E. Visser
    When assessing the benefits of early arrival date of migratory birds, a hidden and often ignored component of males’ fitness is the higher chance of early-arriving birds to obtain extra-pair fertilizations. Here we investigated how extra-pair paternity might affect the relationship between male arrival date and number of fertilizations in a model study system, the European pied flycatcher Ficedula hypoleuca. For this purpose, we sampled and genotyped breeding pairs, unpaired males and offspring (including embryos from unhatched eggs when possible) of a Dutch pied flycatcher population. Detailed information on arrival date of males, egg laying date of their social mates and nest success was also recorded. Early-arriving males had early-laying females and males with early-laying females had a higher probability of siring extra-pair eggs and obtain more fertilizations. However, male arrival date alone did not correlate with the probability to gain extra-pair paternity and neither to the amount of fertilized eggs. Both early- and late-arriving males had a higher probability of losing paternity in their own nest compared to birds with an intermediate arrival date. Finally, late-arriving males were more likely to remain unpaired but, interestingly, a few of these birds obtained paternity via extra-pair copulations. Because earlier arrival date did not lead to more extra-pair fertilizations and because such relationship seems to be driven mainly by the female's laying date, we conclude that the contribution of extra-pair paternity to the overall fitness benefits of early male arrival date is relatively small.
    https://doi.org/10.1111/jav.01317
  • Royal Society Open Science
    11-01-2017

    Experimental illumination of a forest: no effects of lights of different colours on the onset of the dawn chorus in songbirds

    Arnaud Da Silva, Maaike de Jong, Roy H. A. van Grunsven, Marcel E. Visser, Bart Kempenaers, Kamiel Spoelstra
    Light pollution is increasing exponentially, but its impact on animal behaviour is still poorly understood. For songbirds, the most repeatable finding is that artificial night lighting leads to an earlier daily onset of dawn singing. Most of these studies are, however, correlational and cannot entirely dissociate effects of light pollution from other effects of urbanization. In addition, there are no studies in which the effects of different light colours on singing have been tested. Here, we investigated whether the timing of dawn singing in wild songbirds is influenced by artificial light using an experimental set-up with conventional street lights. We illuminated eight previously dark forest edges with white, green, red or no light, and recorded daily onset of dawn singing during the breeding season. Based on earlier work, we predicted that onset of singing would be earlier in the lighted treatments, with the strongest effects in the early-singing species. However, we found no significant effect of the experimental night lighting (of any colour) in the 14 species for which we obtained sufficient data. Confounding effects of urbanization in previous studies may explain these results, but we also suggest that the experimental night lighting may not have been strong enough to have an effect on singing.
    https://doi.org/10.1098/rsos.160638
  • Global Change Biology
    2017

    What type of rigorous experiments are needed to investigate the impact of artificial light at night on individuals and populations?

    Jenny Ouyang, Maaike de Jong, Roy H. A. van Grunsven, Kevin D. Matson, Mark F. Haussmann, Peter Meerlo, Marcel E. Visser, Kamiel Spoelstra
    https://doi.org/10.1111/gcb.13894
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    2017

    Behavioural, ecological and evolutionary response to extreme climatic events: Challenges & directions

    Martijn van de Pol, S. Jenouvrier, J.H.C. Cornelissen, Marcel E. Visser
    More extreme climatic events (ECEs) are among the most prominent consequences of climate change. Despite a long-standing recognition of the importance of ECEs by paleo-ecologists and macro-evolutionary biologists, ECEs have only recently received a strong interest in the wider ecological and evolutionary community. However, as with many rapidly expanding fields, it lacks structure and cohesiveness, which strongly limits scientific progress. Furthermore, due to the descriptive and anecdotal nature of many ECE studies it is still unclear what the most relevant questions and long-term consequences are of ECEs. To improve synthesis, we first discuss ways to define ECEs that facilitate comparison among studies. We then argue that biologists should adhere to more rigorous attribution and mechanistic methods to assess ECE impacts. Subsequently, we discuss conceptual and methodological links with climatology and disturbance-, tipping point- and paleo-ecology. These research fields have close linkages with ECE research, but differ in the identity and/or the relative severity of environmental factors. By summarizing the contributions to this theme issue we draw parallels between behavioural, ecological and evolutionary ECE studies, and suggest that an overarching challenge is that most empirical and theoretical evidence points towards responses being highly idiosyncratic, and thus predictability being low. Finally, we suggest a roadmap based on the proposition that an increased focus on the mechanisms behind the biological response function will be crucial for increased understanding and predictability of the impacts of ECE.
    https://doi.org/10.1098/rstb.2016.0134
  • Global Change Biology
    2017

    Restless roosts: Light pollution affects behavior, sleep, and physiology in a free-living songbird

    Jenny Ouyang, Maaike de Jong, Roy H. A. van Grunsven, Kevin D. Matson, Mark F. Haussmann, Peter Meerlo, Marcel E. Visser, Kamiel Spoelstra
    The natural nighttime environment is increasingly polluted by artificial light. Several studies have linked artificial light at night to negative impacts on human health. In free-living animals, light pollution is associated with changes in circadian, reproductive, and social behavior, but whether these animals also suffer from physiologic costs remains unknown. To fill this gap, we made use of a unique network of field sites which are either completely unlit (control), or are artificially illuminated with white, green, or red light. We monitored nighttime activity of adult great tits, Parus major, and related this activity to within-individual changes in physiologic indices. Because altered nighttime activity as a result of light pollution may affect health and well-being, we measured oxalic acid concentrations as a biomarker for sleep restriction, acute phase protein concentrations and malaria infection as indices of immune function, and telomere lengths as an overall measure of metabolic costs. Compared to other treatments, individuals roosting in the white light were much more active at night. In these individuals, oxalic acid decreased over the course of the study. We also found that individuals roosting in the white light treatment had a higher probability of malaria infection. Our results indicate that white light at night increases nighttime activity levels and sleep debt and affects disease dynamics in a free-living songbird. Our study offers the first evidence of detrimental effects of light pollution on the health of free-ranging wild animals.
    https://doi.org/10.1111/gcb.13756
  • 2017

    Phenological Shifts in Animals Under Contemporary Climate Change

    One of the best documented impacts of climate change has been on the seasonal timing, or phenology, of species. There are clear shifts in all taxonomic groups in terrestrial, aquatic, and marine environments. There is, however, ample variation in the rate at which species shift in response to warmer temperatures. As a consequence, phenological mismatches may occur, in which the phenology of one species no longer matches that of another species, for instance, in predator–prey systems. These mismatches can have an impact on the viability of populations and thereby on biodiversity.
    https://doi.org/10.1016/B978-0-12-809633-8.02301-3
  • Oikos
    12-2016

    Modeling winter moth Operophtera brumata egg phenology: nonlinear effects of temperature and developmental stage on developmental rate

    Lucia Salis, Marjolein Lof, M. Van Asch, Marcel E. Visser
    Understanding the relationship between an insect's developmental rate and temperature is crucial to forecast insect phenology under climate change. In the winter moth Operophtera brumata timing of egg-hatching has severe fitness consequences on growth and reproduction as egg-hatching has to match bud burst of the host tree. In the winter moth, as in many insect species, egg development is strongly affected by ambient temperatures. Here we use laboratory experiments to show for the first time that the effect of temperature on developmental rate depends on the stage of development of the eggs. Building on this experimental finding, we present a novel physiological model to describe winter moth egg development in response to temperature. Our model, a modification of the existing Sharpe-Schoolfield biophysical model, incorporates the effect of developmental stage on developmental rate. Next we validate this model using a 13-year data-set from winter moth eggs kept under ambient conditions and compared this validation with a degree day model and with the Sharpe-Schoolfield model, which lacks the interaction between temperature and developmental stage on developmental rate. We show that accounting for the interaction between temperature and developmental stage improved the predictive power of the model and contributed to our understanding of annual variation in winter moth egg phenology. As climate change leads to unequal changes in temperatures throughout the year, a description of insect development in response to realistic patterns of temperature rather than an invariable degree-day approach will help us to better predict future responses of insect phenology, and thereby insect fitness, to climate change.This article is protected by copyright. All rights reserved.
    https://doi.org/10.1111/oik.03257
  • General and Comparative Endocrinology
    01-09-2016

    Temperature-induced variation in yolk androgen and thyroid hormone levels in avian eggs

    Suvi Ruuskanen, Ton G.G. Groothuis, Sonja Schaper, Veerle M. Darras, Bonnie de Vries, Marcel E. Visser
    Abstract Global warming has substantially changed the environment, but the mechanisms to cope with these changes in animals, including the role of maternal effects, are poorly understood. Maternal effects via hormones deposited in eggs, have important environment-dependent effects on offspring development and fitness: thus females are expected to adjust these hormones to the environment, such as the ambient temperature. Longer-term temperature variation could function as a cue, predicting chick rearing conditions to which yolk hormone levels are adjusted, while short-term temperature variation during egg formation may causally affect hormone transfer to eggs. We studied the effects of ambient temperature on yolk androgens (testosterone and androstenedione) and thyroid hormones (thyroxine and triiodothyronine) in great tits (Parus major) using data from unmanipulated clutches from a wild population and from aviary birds (ad libitum food) exposed to different experimental temperature treatments during five years. Both in the wild and in captivity, longer-term pre-laying ambient temperature was not associated with clutch mean yolk hormone levels, while the way androstenedione and thyroxine levels varied across the laying sequence did associate with pre-laying temperature in the wild. Yolk testosterone levels were positively correlated with short-term temperature (during yolk formation) changes within clutches in both wild and captivity. We also report, for the first time in a wild bird, that yolk thyroxine levels correlated with a key environmental factor: thyroxine levels were negatively correlated with ambient temperature during egg formation. Thus, yolk hormone levels, especially testosterone, seem to be causally affected by ambient temperature. These short-term effects might reflect physiological changes in females with changes in ambient temperature. The adaptive value of the variation with ambient temperatures pre-laying or during egg formation should be studied with hormone manipulations in different thermal environments.
    https://doi.org/10.1016/j.ygcen.2016.05.026
  • PLoS One
    29-06-2016

    Do wild great tits avoid exposure to light at night?

    Maaike de Jong, Jenny Ouyang, Roy H. A. van Grunsven, Marcel E. Visser, Kamiel Spoelstra
    Studies of wild populations have provided important insights into the effects of artificial light at night on organisms, populations and ecosystems. However, in most studies the exact amount of light at night individuals are exposed to remains unknown. Individuals can potentially control their nighttime light exposure by seeking dark spots within illuminated areas. This uncertainty makes it difficult to attribute effects to a direct effect of light at night, or to indirect effects, e.g., via an effect of light at night on food availability. In this study, we aim to quantify the nocturnal light exposure of wild birds in a previously dark forest-edge habitat, experimentally illuminated with three different colors of street lighting, in comparison to a dark control. During two consecutive breeding seasons, we deployed male great tits (Parus major) with a light logger measuring light intensity every five minutes over a 24h period. We found that three males from pairs breeding in brightly illuminated nest boxes close to green and red lamp posts, were not exposed to more artificial light at night than males from pairs breeding further away. This suggests, based on our limited sample size, that these males could have been avoiding light at night by choosing a roosting place with a reduced light intensity. Therefore, effects of light at night previously reported for this species in our experimental set-up might be indirect. In contrast to urban areas where light is omnipresent, bird species in non-urban areas may evade exposure to nocturnal artificial light, thereby avoiding direct consequences of light at night.
    https://doi.org/10.1371/journal.pone.0157357
  • Biological Journal of the Linnean Society
    19-05-2016

    Low but contrasting neutral genetic differentiation shaped by winter temperature in European great tits.

    M. Lemoine, K. Lucek, C. Perrier, V. Saladin, F. Adriaensen, E. Barba, E.J. Belda, A. Charmantier, Mariusz Cichoń, T. Eeva, A. Grégoire, C.A. Hinde, Arild Johnsen, J. Komdeur, R. Mänd, Erik Matthysen, Ana C. Norte, N. Pitala, Ben C. Sheldon, T. Slagsvold, J.M. Tinbergen, J. Török, R. Ubels, Kees van Oers, Marcel E. Visser, Blandine F. Doligez, Heinz Richner
    Gene flow is usually thought to reduce genetic divergence and impede local adaptation by homogenising gene pools between populations. However, evidence for local adaptation and phenotypic differentiation in highly mobile species, experiencing high levels of gene flow, is emerging. Assessing population genetic structure at different spatial scales is thus a crucial step towards understanding mechanisms underlying intraspecific differentiation and diversification. Here, we studied the population genetic structure of a highly mobile species – the great tit Parus major – at different spatial scales. We analysed 884 individuals from 30 sites across Europe including 10 close-by sites (< 50 km), using 22 microsatellite markers. Overall we found a low but significant genetic differentiation among sites (FST = 0.008). Genetic differentiation was higher, and genetic diversity lower, in south-western Europe. These regional differences were statistically best explained by winter temperature. Overall, our results suggest that great tits form a single patchy metapopulation across Europe, in which genetic differentiation is independent of geographical distance and gene flow may be regulated by environmental factors via movements related to winter severity. This might have important implications for the evolutionary trajectories of sub-populations, especially in the context of climate change, and calls for future investigations of local differences in costs and benefits of philopatry at large scales.
    https://doi.org/10.1111/bij.12745
  • Hormones and Behavior
    05-2016

    Effects of experimentally manipulated yolk thyroid hormone levels on offspring development in a wild bird species

    Suvi Ruuskanen, Veerle M. Darras, Marcel E. Visser, Ton G.G. Groothuis
    Abstract Maternal effects are a crucial mechanism in a wide array of taxa to generate phenotypic variation, thereby affecting offspring development and fitness. Maternally derived thyroid hormones (THs) are known to be essential for offspring development in mammalian and fish models, but have been largely neglected in avian studies, especially in respect to natural variation and an ecological context. We studied, for the first time in a wild species and population, the effects of maternally derived THs on offspring development, behavior, physiology and fitness-related traits by experimental elevation of thyroxine and triiodothyronine in ovo within the physiological range in great tits (Parus major). We found that elevated yolk TH levels had a sex-specific effect on growth, increasing male and decreasing female growth, relative to controls, and this effect was similar throughout the nestling period. Hatching or fledging success, motor coordination behavior, stress reactivity and resting metabolic rate were not affected by the TH treatment. We conclude that natural variation in maternally derived THs may affect some offspring traits in a wild species. As this is the first study on yolk thyroid hormones in a wild species and population, more such studies are needed to investigate its effects on pre-hatching development, and juvenile and adult fitness before generalizations on the importance of maternally derived yolk thyroid hormones can be made. However, this opens a new, interesting avenue for further research in the field of hormone mediated maternal effects.
    https://doi.org/10.1016/j.yhbeh.2016.03.006
  • Trends in Ecology & Evolution
    02-2016

    Solutions for Archiving Data in Long-Term Studies

    James A Mills, Céline Teplitsky, Beatriz Arroyo, Anne Charmantier, Peter H Becker, Tim R Birkhead, Pierre Bize, Daniel T. Blumstein, Christophe Bonenfant, Stan Boutin, Andrey Bushuev, Emmanuelle Cam, Andrew Cockburn, Steeve D Côté, John C Coulson, Francis Daunt, N.J. Dingemanse, Blandine F. Doligez, Hugh Drummond, Richard H. M. Espie, Marco Festa-Bianchet, Francesca D. Frentiu, John W. Fitzpatrick, Robert W. Furness, G. Gauthier, Peter R. Grant, Michael Griesser, Lars Gustafsson, Bengt Hansson, Michael P. Harris, Frédéric Jiguet, Petter Kjellander, Erkki Korpimäki, Charles J Krebs, Luc Lens, John D C Linnell, Matthew Low, Andrew G. McAdam, Antoni Margalida, Juha Merilä, Anders P. Møller, Shinichi Nakagawa, Jan-Åke Nilsson, Ian C. T. Nisbet, Arie Van Noordwijk, Daniel Oro, Tomas Pärt, Fanie Pelletier, Jaime Potti, Benoit Pujol, Denis Réale, Robert F Rockwell, Yan Ropert-Coudert, Alexandre Roulin, Christophe Thébaud, James S. Sedinger, Jon E. Swenson, Marcel E. Visser, Sarah Wanless, David F Westneat, Alastair J Wilson, Andreas Zedrosser
    https://doi.org/10.1016/j.tree.2015.12.004
  • Heredity
    2016

    Heritable variation in maternally derived yolk androgens, thyroid hormones and immune factors

    Suvi Ruuskanen, Phillip Gienapp, T.G.G. Groothuis, Sonja Schaper, Veerle M. Darras, Cheila Pereira, Bonnie de Vries, Marcel E. Visser
    Maternal reproductive investment can critically influence offspring phenotype, and thus these maternal effects are expected to be under strong natural selection. Knowledge on the extent of heritable variation in the physiological mechanisms underlying maternal effects is however limited. In birds, resource allocation to eggs is a key mechanism for mothers to affect their offspring and different components of the egg may or may not be independently adjusted. We studied the heritability of egg components and their genetic and phenotypic covariation in great tits (Parus major), using captive-bred full siblings of wild origin. Egg mass, testosterone (T) and androstenedione (A4) hormone concentrations showed moderate heritability, in agreement with earlier findings. Interestingly, yolk triiodothyronine hormone (T3), but not its precursor, thyroxine hormone (T4), concentration was heritable. An immune factor, albumen lysozyme, showed moderate heritability, but yolk immunoglobulins (IgY) did not. The genetic correlation estimates were moderate but statistically nonsignificant; a trend for a positive genetic correlation was found between A4 and egg mass, T and lysozyme and IgY and lysozyme, respectively. Interestingly, phenotypic correlations were found only between A4 and T, and T4 and T3, respectively. Given that these egg components are associated with fitness-related traits in the offspring (and mother), and that we show that some components are heritable, it opens the possibility that natural selection may shape the rate and direction of phenotypic change via egg composition.
    https://doi.org/10.1038/hdy.2016.49
  • Evolution
    2016

    Testing for biases in selection on avian reproductive traits and partitioning direct and indirect selection using quantitative genetic models

    Thomas Reed, Phillip Gienapp, Marcel E. Visser
    ey life history traits such as breeding time and clutch size are frequently both heritable and under directional selection, yet many studies fail to document micro-evolutionary responses. One general explanation is that selection estimates are biased by the omission of correlated traits that have causal effects on fitness, but few valid tests of this exist. Here we show, using a quantitative genetic framework and six decades of life-history data on two free-living populations of great tits Parus major, that selection estimates for egg-laying date and clutch size are relatively unbiased. Predicted responses to selection based on the Robertson-Price Identity were similar to those based on the multivariate breeder's equation, indicating that unmeasured covarying traits were not missing from the analysis. Changing patterns of phenotypic selection on these traits (for laying date, linked to climate change) therefore reflect changing selection on breeding values, and genetic constraints appear not to limit their independent evolution. Quantitative genetic analysis of correlational data from pedigreed populations can be a valuable complement to experimental approaches to help identify whether apparent associations between traits and fitness are biased by missing traits, and to parse the roles of direct versus indirect selection across a range of environments.
    https://doi.org/10.1111/evo.13017
  • Proceedings of the Royal Society B-Biological Sciences
    2016

    Climate change relaxes the time constraints for late-born offspring in a long-distance migrant

    Barbara Tomotani, Phillip Gienapp, Domien G. M. Beersma, Marcel E. Visser
    Animals in seasonal environments need to fit their annual-cycle stages, such as moult and migration, in a tight schedule. Climate change affects the phenology of organisms and causes advancements in timing of these annual-cycle stages but not necessarily at the same rates. For migratory birds, this can lead to more severe or more relaxed time constraints in the time from fledging to migration, depending on the relative shifts of the different stages. We tested how a shift in hatch date, which has advanced due to climate change, impacts the organization of the birds' whole annual cycle. We experimentally advanced and delayed the hatch date of pied flycatcher chicks in the field and then measured the timing of their annual-cycle stages in a controlled laboratory environment. Hatch date affected the timing of moult and pre-migratory fattening, but not migration. Early-born birds hence had a longer time to fatten up than late-born ones; the latter reduced their interval between onset of fattening and migration to be able to migrate at the same time as the early-born birds. This difference in time constraints for early- and late-born individuals may explain why early-born offspring have a higher probability to recruit as a breeding bird. Climate change-associated advancements of avian egg-lay dates, which in turn advances hatch dates, can thus reduce the negative fitness consequences of reproducing late, thereby reducing the selection for early egg-laying migratory birds.
    https://doi.org/10.1098/rspb.2016.1366
  • Evolution
    2016

    Genetic variation in variability: phenotypic variability of fledging weight and its evolution in a songbird population

    HA Mulder, Phillip Gienapp, Marcel E. Visser
    Variation in traits is essential for natural selection to operate and genetic and environmental effects can contribute to this phenotypic variation. From domesticated populations, we know that families can differ in their level of within-family variance, which leads to the intriguing situation that within-family variance can be heritable. For offspring traits, such as birth weight, this implies that within-family variance in traits can vary among families and can thus be shaped by natural selection. Empirical evidence for this in wild populations is however lacking. We investigated whether within-family variance in fledging weight is heritable in a wild great tit (Parus major) population and whether these differences are associated with fitness. We found significant evidence for genetic variance in within-family variance. The genetic coefficient of variation (GCV) was 0.18 and 0.25, when considering fledging weight a parental or offspring trait, respectively. We found a significant quadratic relationship between within-family variance and fitness: families with low or high within-family variance had lower fitness than families with intermediate within-family variance. Our results show that within-family variance can respond to selection and provides evidence for stabilizing selection on within-family variance.
    https://doi.org/10.1111/evo.13008
  • Nature Communications
    2016

    Demographic routes to variability and regulation in bird populations

    Bernt-Erik Sæther, Vidar Grøtan, Steinar Engen, Tim Coulson, Peter R. Grant, Marcel E. Visser, Jon E Brommer, B Rosemary Grant, Lars Gustafsson, Ben J Hatchwell, Kurt Jerstad, Patrik Karell, Hannu Pietiäinen, Alexandre Roulin, Ole W Røstad, Henri Weimerskirch
    There is large interspecific variation in the magnitude of population fluctuations, even among closely related species. The factors generating this variation are not well understood, primarily because of the challenges of separating the relative impact of variation in population size from fluctuations in the environment. Here, we show using demographic data from 13 bird populations that magnitudes of fluctuations in population size are mainly driven by stochastic fluctuations in the environment. Regulation towards an equilibrium population size occurs through density-dependent mortality. At small population sizes, population dynamics are primarily driven by environment-driven variation in recruitment, whereas close to the carrying capacity K, variation in population growth is more strongly influenced by density-dependent mortality of both juveniles and adults. Our results provide evidence for the hypothesis proposed by Lack that population fluctuations in birds arise from temporal variation in the difference between density-independent recruitment and density-dependent mortality during the non-breeding season.
    https://doi.org/10.1038/ncomms12001
  • Journal of Avian Biology
    2016

    Experimental manipulation of food availability leads to short-term intra-clutch adjustment in egg mass but not in yolk androgen or thyroid hormones.

    Suvi Ruuskanen, Veerle M. Darras, Bonnie de Vries, Marcel E. Visser, T.G.G. Groothuis
    In birds, mothers can affect their offspring's phenotype and thereby survival via egg composition. It is not well known to what extent and time-scales environmental variation in resource availability, either via resource constrains or adaptive adjustment to predicted rearing conditions, influences maternal effects. We experimentally studied whether egg and yolk mass and yolk hormone levels respond to short-term changes in food availability during laying in wild great tits (Parus major). Our treatment groups were: 1) food supplementation (mealworms) from the 1st until the last egg; 2) food supplementation from the 1st first until the 5th egg, where the effect of cessation of the supplementary food treatment could also be studied; 3) no food supplementation (controls). We analysed both nutritional resources (egg, yolk and albumen mass), and the important developmental signals, yolk androgens (testosterone and androstenedione), and for the first time in a wild population, yolk thyroid hormones (thyroxine and 3,5,3’-triiodothyronine). Egg mass is a costly resource for females, androgens most likely non-costly signals, whereas thyroid hormones may be costly signals, requiring environmental iodine. In the food supplemented group egg, yolk and albumen mass increased rapidly relative to controls and when food supplementation was halted, egg and albumen mass decreased, indicating rapid responses to resource availability. Yolk androgen and thyroid hormone levels were not affected by food supplementation during laying. Thyroxine showed an increase over the laying sequence and its biological meaning needs further study. The rapid changes in egg mass to variation in within-clutch food availability suggest energetic/protein/nutrient constrains on egg formation. The lack of a response in yolk hormones suggest that perhaps in this species the short-term changes in resource availability during egg laying do not predict offspring rearing conditions, or (for thyroid hormones) do not cause systemic changes in circulating hormones, and hence do not affect maternal signaling.
    https://doi.org/10.1111/jav.00728
  • Physiology & Behavior
    2016

    Dose-dependent responses of avian daily rhythms to artificial light at night

    Maaike de Jong, Lizanne Jeninga, Jenny Ouyang, Kees van Oers, Kamiel Spoelstra, Marcel E. Visser
    Recent studies have shown that animals are affected by night-time light exposure. Light is a continuous variable, but our knowledge on how individuals react to different light intensities during the night is limited. We therefore determined the relationship between night light intensity and the behaviour and physiology of great tits (Parus major). We measured daily activity patterns and melatonin levels in 35 males exposed to five different light intensities and found strong, dose-dependent effects. Activity onset was increasingly advanced, and activity offset delayed with higher light intensities. Furthermore, night-time activity increased and melatonin levels measured at midnight decreased with higher intensities. In this experimental study, we demonstrate for the first time dose-dependent effects of artificial light at night on birds' daily activity patterns and melatonin levels. Our results imply that these effects are not limited to a certain threshold, but emerge even when nocturnal light levels are slightly increased. However, in a natural area, these effects may be limited as artificial light levels are commonly low; light intensities drop rapidly with distance from a light source and birds can avoid exposure to light at night. Future studies should thus focus on examining the impact of different intensities of light at night in the wild.
    https://doi.org/10.1016/j.physbeh.2015.12.012
  • Nature Communications
    2016

    Evolutionary signals of selection on cognition from the great tit genome and methylome

    Veronika Laine, Toni I. Gossmann, K.M. Schachtschneider, Colin J. Garroway, Ole Madsen, Koen Verhoeven, Victor de Jager, H-J. Megens, W.C. Warren, P. Minx, R.P.M.A. Crooijmans, Pádraic Corcoran, Ben C. Sheldon, J. Slate, Kai Zeng, Kees van Oers, Marcel E. Visser, M.A.M. Groenen
    For over 50 years, the great tit (Parus major) has been a model species for research in evolutionary, ecological and behavioural research; in particular, learning and cognition have been intensively studied. Here, to provide further insight into the molecular mechanisms behind these important traits, we de novo assemble a great tit reference genome and whole-genome re-sequence another 29 individuals from across Europe. We show an overrepresentation of genes related to neuronal functions, learning and cognition in regions under positive selection, as well as increased CpG methylation in these regions. In addition, great tit neuronal non-CpG methylation patterns are very similar to those observed in mammals, suggesting a universal role in neuronal epigenetic regulation which can affect learning-, memory- and experience-induced plasticity. The high-quality great tit genome assembly will play an instrumental role in furthering the integration of ecological, evolutionary, behavioural and genomic approaches in this model species.
    https://doi.org/10.1038/ncomms10474
  • Ecology
    2016

    Density dependence in an age-structured population of great tits: identifying the critical age classes

    Marlène Gamelon, V. Grotan, S. Engen, E. Bjørkvoll, Marcel E. Visser, Bernt-Erik Sæther
    Classical approaches for the analyses of density dependence assume that all the individuals in a population equally respond and equally contribute to density dependence. However, in age-structured populations, individuals of different ages may differ in their responses to changes in population size and how they contribute to density dependence affecting the growth rate of the whole population. Here, we apply the concept of critical age classes, i.e., a specific scalar function that describes how one or a combination of several age classes affect the demographic rates negatively, in order to examine how total density dependence acting on the population growth rate depends on the age-specific population sizes. In a 38-year dataset of an age-structured great tit (Parus major) population, we find that the age classes including the youngest breeding females were the critical age classes for density regulation. These age classes correspond to new breeders that attempt to take a territory and that have the strongest competitive effect on other breeding females. They strongly affected population growth rate and reduced recruitment and survival rates of all breeding females. We also show that depending on their age class, females may differently respond to varying density. In particular, the negative effect of the number of breeding females was stronger on recruitment rate of the youngest breeding females. These findings question the classical assumptions that all the individuals of a population can be treated as having an equal contribution to density regulation and that the effect of the number of individuals is age independent. Our results improve our understanding of density regulation in natural populations.
    https://doi.org/10.1002/ecy.1442
  • Proceedings of the Royal Society B-Biological Sciences
    2016

    Evidence for r- and K-selection in a wild bird population: a reciprocal link between ecology and evolution.

    S.A. Saether, Marcel E. Visser, V. Grotan, S. Engen
    Understanding the variation in selection pressure on key life-history traits is crucial in our rapidly changing world. Density is rarely considered as a selective agent. To study its importance, we partition phenotypic selection in fluctuating environments into components representing the population growth rate at low densities and the strength of density dependence, using a new stochastic modelling framework. We analysed the number of eggs laid per season in a small song-bird, the great tit, and found balancing selection favouring large clutch sizes at small population densities and smaller clutches in years with large populations. A significant interaction between clutch size and population size in the regression for the Malthusian fitness reveals that those females producing large clutch sizes at small population sizes also are those that show the strongest reduction in fitness when population size is increased. This provides empirical support for ongoing r- and K-selection in this population, favouring phenotypes with large growth rates r at small population sizes and phenotypes with high competitive skills when populations are close to the carrying capacity K. This selection causes long-term fluctuations around a stable mean clutch size caused by variation in population size, implying that r- and K-selection is an important mechanism influencing phenotypic evolution in fluctuating environments. This provides a general link between ecological dynamics and evolutionary processes, operating through a joint influence of density dependence and environmental stochasticity on fluctuations in population size.
    https://doi.org/10.1098/rspb.2015.2411
  • Molecular Ecology
    12-2015

    Replicated analysis of the genetic architecture of quantitative traits in two wild great tit populations.

    A.W. Santure, Jocelyn Poissant, I. de Cauwer, Kees van Oers, M.R. Robinson, J.L. Quinn, M.A.M. Groenen, Marcel E. Visser, Ben C. Sheldon, J. Slate
    Currently, there is much debate on the genetic architecture of quantitative traits in wild populations. Is trait variation influenced by many genes of small effect or by a few genes of major effect? Where is additive genetic variation located in the genome? Do the same loci cause similar phenotypic variation in different populations? Great tits (Parus major) have been studied extensively in long-term studies across Europe and consequently are considered an ecological ‘model organism’. Recently, genomic resources have been developed for the great tit, including a custom SNP chip and genetic linkage map. In this study, we used a suite of approaches to investigate the genetic architecture of eight quantitative traits in two long-term study populations of great tits—one in the Netherlands and the other in the United Kingdom. Overall, we found little evidence for the presence of genes of large effects in either population. Instead, traits appeared to be influenced by many genes of small effect, with conservative estimates of the number of contributing loci ranging from 31 to 310. Despite concordance between population-specific heritabilities, we found no evidence for the presence of loci having similar effects in both populations. While population-specific genetic architectures are possible, an undetected shared architecture cannot be rejected because of limited power to map loci of small and moderate effects. This study is one of few examples of genetic architecture analysis in replicated wild populations and highlights some of the challenges and limitations researchers will face when attempting similar molecular quantitative genetic studies in free-living populations
    https://doi.org/10.1111/mec.13452
  • Proceedings of the Royal Society B-Biological Sciences
    22-05-2015

    Testing for effects of climate change on competitive relationships and coexistence between two bird species

    Nils Chr. Stenseth, Joel M. Durant, Mike S. Fowler, Erik Matthysen, Frank Adriaensen, Niclas Jonzen, Kung-Sik Chan, Hai Liu, Jenny De Laet, Ben C. Sheldon, Marcel E. Visser, André A Dhondt
    Climate change is expected to have profound ecological effects, yet shifts in competitive abilities among species are rarely studied in this context. Blue tits (Cyanistes caeruleus) and great tits (Parus major) compete for food and roosting sites, yet coexist across much of their range. Climate change might thus change the competitive relationships and coexistence between these two species. Analysing four of the highest-quality, long-term datasets available on these species across Europe, we extend the textbook example of coexistence between competing species to include the dynamic effects of long-term climate variation. Using threshold time-series statistical modelling, we demonstrate that long-term climate variation affects species demography through different influences on density-dependent and density-independent processes. The competitive interaction between blue tits and great tits has shifted in one of the studied sites, creating conditions that alter the relative equilibrium densities between the two species, potentially disrupting long-term coexistence. Our analyses show that long-term climate change can, but does not always, generate local differences in the equilibrium conditions of spatially structured species assemblages. We demonstrate how long-term data can be used to better understand whether (and how), for instance, climate change might change the relationships between coexisting species. However, the studied populations are rather robust against competitive exclusion.
    https://doi.org/10.1098/rspb.2014.1958
  • PLoS Biology
    07-04-2015

    Effects of Spring Temperatures on the Strength of Selection on Timing of Reproduction in a Long-Distance Migratory Bird

    Marcel E. Visser, Phillip Gienapp, Arild Husby, Michael Morrisey, Iván De la Hera, F. Pulido, Christiaan Both

    A 31-year study of pied flycatchers shows that it is the temperature at arrival when the offspring return to breed up to two years later that drives selection on breeding time.

    Climate change has differentially affected the timing of seasonal events for interacting trophic levels, and this has often led to increased selection on seasonal timing. Yet, the environmental variables driving this selection have rarely been identified, limiting our ability to predict future ecological impacts of climate change. Using a dataset spanning 31 years from a natural population of pied flycatchers (Ficedula hypoleuca), we show that directional selection on timing of reproduction intensified in the first two decades (1980–2000) but weakened during the last decade (2001–2010). Against expectation, this pattern could not be explained by the temporal variation in the phenological mismatch with food abundance. We therefore explored an alternative hypothesis that selection on timing was affected by conditions individuals experience when arriving in spring at the breeding grounds: arriving early in cold conditions may reduce survival. First, we show that in female recruits, spring arrival date in the first breeding year correlates positively with hatch date; hence, early-hatched individuals experience colder conditions at arrival than late-hatched individuals. Second, we show that when temperatures at arrival in the recruitment year were high, early-hatched young had a higher recruitment probability than when temperatures were low. We interpret this as a potential cost of arriving early in colder years, and climate warming may have reduced this cost. We thus show that higher temperatures in the arrival year of recruits were associated with stronger selection for early reproduction in the years these birds were born. As arrival temperatures in the beginning of the study increased, but recently declined again, directional selection on timing of reproduction showed a nonlinear change. We demonstrate that environmental conditions with a lag of up to two years can alter selection on phenological traits in natural populations, something that has important implications for our understanding of how climate can alter patterns of selection in natural populations.

    https://doi.org/10.1371/journal.pbio.1002120
  • Evolution
    2015

    Estimating the variation, autocorrelation, and environmental sensitivity of phenotypic selection

    Luis-Miguel Chevin, Marcel E. Visser, Jarle Tufto
    Despite considerable interest in temporal and spatial variation of phenotypic selection, very few methods allow quantifying this variation while correctly accounting for the error variance of each individual estimate. Furthermore, the available methods do not estimate the autocorrelation of phenotypic selection, which is a major determinant of eco-evolutionary dynamics in changing environments. We introduce a new method for measuring variable phenotypic selection using random regression. We rely on model selection to assess the support for stabilizing selection, and for a moving optimum that may include a trend plus (possibly autocorrelated) fluctuations. The environmental sensitivity of selection also can be estimated by including an environmental covariate. After testing our method on extensive simulations, we apply it to breeding time in a great tit population in the Netherlands. Our analysis finds support for an optimum that is well predicted by spring temperature, and occurs about 33 days before a peak in food biomass, consistent with what is known from the biology of this species. We also detect autocorrelated fluctuations in the optimum, beyond those caused by temperature and the food peak. Because our approach directly estimates parameters that appear in theoretical models, it should be particularly useful for predicting eco-evolutionary responses to environmental change.
    https://doi.org/10.1111/evo.12741
  • Philosophical Transactions of the Royal Society B
    2015

    Effects of nocturnal illumination on life-history decisions and fitness in two wild songbird species

    Maaike de Jong, Jenny Ouyang, Arnaud Da Silva, Roy H. A. van Grunsven, Bart Kempenaers, Marcel E. Visser, Kamiel Spoelstra
    The effects of artificial night lighting on animal behaviour and fitness are largely unknown. Most studies report short-term consequences in locations that are also exposed to other anthropogenic disturbance. We know little about how the effects of nocturnal illumination vary with different light colour compositions. This is increasingly relevant as the use of LED lights becomes more common, and LED light colour composition can be easily adjusted. We experimentally illuminated previously dark natural habitat with white, green and red light, and measured the effects on life-history decisions and fitness in two free-living songbird species, the great tit (Parus major) and pied flycatcher (Ficedula hypoleuca) in two consecutive years. In 2013, but not in 2014, we found an effect of light treatment on lay date, and of the interaction of treatment and distance to the nearest lamp post on chick mass in great tits but not in pied flycatchers. We did not find an effect in either species of light treatment on breeding densities, clutch size, probability of brood failure, number of fledglings and adult survival. The finding that light colour may have differential effects opens up the possibility to mitigate negative ecological effects of nocturnal illumination by using different light spectra. artificial light at nightlight spectralife-historyfitnessParus majorFicedula hypoleucaFootnotesOne contribution of 14 to a theme issue ‘The biological impacts of artificial light at night: from molecules to communities’.© 2015 The Author(s) Published by the Royal Society. All rights reserved.
    https://doi.org/10.1098/rstb.2014.0128
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    2015

    Experimental illumination of natural habitat—an experimental set-up to assess the direct and indirect ecological consequences of artificial light of different spectral composition

    Kamiel Spoelstra, Roy H. A. van Grunsven, Maurice Donners, Phillip Gienapp, Martinus E. Huigens, Roy Slaterus, Frank Berendse, Marcel E. Visser, Elmar M. Veenendaal
    Artificial night-time illumination of natural habitats has increased dramatically over the past few decades. Generally, studies that assess the impact of artificial light on various species in the wild make use of existing illumination and are therefore correlative. Moreover, studies mostly focus on short-term consequences at the individual level, rather than long-term consequences at the population and community level—thereby ignoring possible unknown cascading effects in ecosystems. The recent change to LED lighting has opened up the exciting possibility to use light with a custom spectral composition, thereby potentially reducing the negative impact of artificial light. We describe here a large-scale, ecosystem-wide study where we experimentally illuminate forest-edge habitat with different spectral composition, replicated eight times. Monitoring of species is being performed according to rigid protocols, in part using a citizen-science-based approach, and automated where possible. Simultaneously, we specifically look at alterations in behaviour, such as changes in activity, and daily and seasonal timing. In our set-up, we have so far observed that experimental lights facilitate foraging activity of pipistrelle bats, suppress activity of wood mice and have effects on birds at the community level, which vary with spectral composition. Thus far, we have not observed effects on moth populations, but these and many other effects may surface only after a longer period of time. experimental lightingpopulation dynamicsdaily timingseasonal timingcascading effectscitizen scienceFootnotesOne contribution of 14 to a theme issue ‘The biological impacts of artificial light at night: from molecules to communities’.© 2015 The Author(s) Published by the Royal Society. All rights reserved.
    https://doi.org/10.1098/rstb.2014.0129
  • Proceedings of the Royal Society B-Biological Sciences
    2015

    Disrupted seasonal biology impacts health, food security, and ecosystems: a call for integrated research

    T.J. Stevenson, Marcel E. Visser, Walter Arnold, P Barrett, S. Biello, A. Dawson, D.L. Denlinger, Davide Dominoni, F.J. Ebling, S. Elton, N. Evans, H.M. Ferguson, Russell Foster, Michaela Hau, D.T. Haydon, D.G. Hazlerigg, P. Heideman, J.G.C. Hopcraft, N.N. Jonsson, Noga Kronfeld-Schor, V. Kumar, G.A. Lincoln, R. MacLeod, S.A.M. Martin, M. Martinez-Bakker, Randy J. Nelson, Thomas Reed, J.E. Robinso, D. Rock, William Schwartz, I. Steffan-Dewenter, E. Tauber, Stephen J. Thackeray, C. Umstatter, T. Yoshimura, B. Helm
    The rhythm of life on earth is shaped by seasonal changes in the environment. Plants and animals show profound annual cycles in physiology, health, morphology, behaviour and demography in response to environmental cues. Seasonal biology impacts ecosystems and agriculture, with consequences for humans and biodiversity. Human populations show robust annual rhythms in health and well-being, and the birth month can have lasting effects that persist throughout life. This review emphasizes the need for a better understanding of seasonal biology against the backdrop of its rapidly progressing disruption through climate change, human lifestyles and other anthropogenic impact. Climate change is modifying annual rhythms to which numerous organisms have adapted, with potential consequences for industries relating to health, ecosystems and food security. Disconcertingly, human lifestyles under artificial conditions of eternal summer provide the most extreme example for disconnect from natural seasons, making humans vulnerable to increased morbidity and mortality. In this review, we introduce scenarios of seasonal disruption, highlight key aspects of seasonal biology and summarize from biomedical, anthropological, veterinary, agricultural and environmental perspectives the recent evidence for seasonal desynchronization between environmental factors and internal rhythms. Because annual rhythms are pervasive across biological systems, they provide a common framework for trans-disciplinary research.
    https://doi.org/10.1098/rspb.2015.1453
  • Genome Biology and Evolution
    2015

    The genome of the winter moth (Operophtera brumata) provides a genomic perspective on sexual dimorphism and phenology

    M. Derks, Sandra Smit, Lucia Salis, Elio G.W.M. Schijlen, Alex Bossers, A.C. Mateman, Agata Pijl, A. De Ridder, M.A.M. Groenen, Marcel E. Visser, H-J. Megens
    The winter moth (Operophtera brumata) belongs to one of the most species-rich families in Lepidoptera, the Geometridae (approx. 23,000 species). This family is of great economic importance as most species are herbivorous and capable of defoliating trees. Genome assembly of the winter moth allows the study of genes and gene families, such as the cytochrome P450 gene family, which is known to be vital in plant secondary metabolite detoxification and host plant selection. It also enables exploration of the genomic basis for female brachyptery (wing reduction), a feature of sexual dimorphism in winter moth, and for seasonal timing, a trait extensively studied in this species. Here we present a reference genome for the winter moth, the first geometrid and largest sequenced Lepidopteran genome to date (638 Mb) including a set of 16,912 predicted protein-coding genes. This allowed us to assess the dynamics of evolution on a genome wide scale using the P450 gene family. We also identified an expanded gene family potentially linked to female brachyptery, and annotated the genes involved in the circadian clock mechanism as main candidates for involvement in seasonal timing. The genome will contribute to Lepidopteran genomic resources and comparative genomics. In addition, the genome enhances our ability to understand the genetic and molecular basis of insect seasonal timing and thereby provides a reference for future evolutionary and population studies on the winter moth.
    https://doi.org/10.1093/gbe/evv145
  • Trends in Ecology & Evolution
    2015

    Archiving primary data: solutions for long-term studies

    James A Mills, Céline Teplitsky, Beatriz Arroyo, A. Charmantier, P. H. Becker, T.R. Birkhead, P. Bize, Daniel T. Blumstein, C. Bonenfant, Stan Boutin, Andrey Bushuev, E. Cam, A. Cockburn, S.D. Côté, J.C. Coulson, F. Daunt, N.J. Dingemanse, Blandine F. Doligez, Hugh Drummond, Richard H. M. Espie, M. Festa-Bianchet, Francesca D. Frentiu, John W. Fitzpatrick, Robert W. Furness, D. Garant, G. Gauthier, Peter R. Grant, Michael Griesser, L. Gustafsson, Bengt Hansson, Michael P. Harris, F. Jiguet, Petter Kjellander, E. Korpimäki, Charles J Krebs, Luc Lens, John D C Linnell, Matthew Low, Andrew G. McAdam, Antoni Margalida, J. Merilä, Anders P. Møller, Shinichi Nakagawa, J.-Å. Nilsson, Ian C. T. Nisbet, Arie Van Noordwijk, Daniel Oro, Tomas Pärt, Fanie Pelletier, J. Potti, Benoit Pujol, Denis Réale, R.F. Rockwell, Yan Ropert-Coudert, Alexandre Roulin, Christophe Thébaud, James S. Sedinger, Jon E. Swenson, Marcel E. Visser, D.F. S.Wanless Westneat, Alastair J Wilson, Andreas Zedrosser
    The recent trend for journals to require open access to primary data included in publications has been embraced by many biologists, but has caused apprehension amongst researchers engaged in long-term ecological and evolutionary studies. A worldwide survey of 73 principal investigators (Pls) with long-term studies revealed positive attitudes towards sharing data with the agreement or involvement of the PI, and 93% of PIs have historically shared data. Only 8% were in favor of uncontrolled, open access to primary data while 63% expressed serious concern. We present here their viewpoint on an issue that can have non-trivial scientific consequences. We discuss potential costs of public data archiving and provide possible solutions to meet the needs of journals and researchers.
    https://doi.org/10.1016/j.tree.2015.07.006
  • Biology Letters
    2015

    Stressful colours: corticosterone concentrations in a free-living songbird vary with the spectral composition of experimental illumination

    Jenny Ouyang, Maaike de Jong, Michaela Hau, Marcel E. Visser, Roy H. A. van Grunsven, Kamiel Spoelstra
    Organisms have evolved under natural daily light/dark cycles for millions of years. These cycles have been disturbed as night-time darkness is increasingly replaced by artificial illumination. Investigating the physiological consequences of free-living organisms in artificially lit environments is crucial to determine whether nocturnal lighting disrupts circadian rhythms, changes behaviour, reduces fitness and ultimately affects population numbers. We make use of a unique, large-scale network of replicated field sites which were experimentally illuminated at night using lampposts emanating either red, green, white or no light to test effect on stress hormone concentrations (corticosterone) in a songbird, the great tit (Parus major). Adults nesting in white-light transects had higher corticosterone concentrations than in the other treatments. We also found a significant interaction between distance to the closest lamppost and treatment type: individuals in red light had higher corticosterone levels when they nested closer to the lamppost than individuals nesting farther away, a decline not observed in the green or dark treatment. Individuals with high corticosterone levels had fewer fledglings, irrespective of treatment. These results show that artificial light can induce changes in individual hormonal phenotype. As these effects vary considerably with light spectrum, it opens the possibility to mitigate these effects by selecting street lighting of specific spectra.
    https://doi.org/10.1098/rsbl.2015.0517
  • Oikos
    2015

    Density dependence and microevolution interactively determine effects of phenology mismatch on population dynamics

    Thomas Reed, Phillip Gienapp, Marcel E. Visser
    Life cycle events in plants and animals are typically adaptively tuned to anticipate predictable seasonal changes in environmental conditions or resources. Climate change is expected to affect the temporal component of species’ interactions, e.g. by creating a mismatch between a predator's breeding time (when ample food supply is critical) and the time when prey abundance is high. The demographic implications of such a mismatch remain unclear, however. Here we focussed on changes in the phenology of consumers relative to that of their food. We developed a model where reproductive output of the consumer up to offspring independence depended on mismatch and recruitment of the offspring to breeders depended on offspring density according to a Beverton–Holt function. Using a deterministic version of the model, we clarified how the effects of (constant) mismatch on equilibrium population size depended on the emergent strength of negative density dependence (DD). Using a stochastic, individual-based version, we showed that when the environment changed abruptly, the rate of population recovery was faster when heritability of seasonal timing was higher and DD was stronger. When the environment shifted continuously, the rate of decline in population size was inversely proportional to the rate of microevolution, but stronger DD slowed the rate of decline for a given heritability and thus effectively ‘bought time’ for evolutionary rescue. These results highlight the importance of negative DD, which interacts with the effects of trait heritability and stabilizing selection strength, in influencing the fate of populations experiencing environmental change. We emphasize, however, that outcomes in nature will depend crucially on the exact nature of DD, in particular whether population growth rate differences are greatest at low or high densities, highlighting the need for empirical comparisons of compensatory processes in different populations or species.
    https://doi.org/10.1111/oik.01398
  • Environmental Science and Pollution Research
    2014

    Large-scale geographical variation in eggshell heavy metal and calcium content in a passerine bird (Ficedula hypoleuca)

    Suvi Ruuskanen, J. Morales, T. Laaksonen, J. Moreno, R. Mateo, Eugen Belskii, Andrey Bushuev, A. Jarvinen, A. Kerimov, I. Krams, C. Morosinotto, R. Mand, M. Orell, A. Qvarnstrom, F.M. Slater, H. Siitari, V. Tilgar, Marcel E. Visser, W. Winkel, H. Zang, T. Eeva
    Birds have been used as bioindicators of pollution, such as toxic metals. Levels of pollutants in eggs are especially interesting, as developing birds are more sensitive to detrimental effects of pollutants than adults. Only very few studies have monitored intraspecific, large-scale variation in metal pollution across a species' breeding range. We studied large-scale geographic variation in metal levels in the eggs of a small passerine, the pied flycatcher (Ficedula hypoleuca), sampled from 15 populations across Europe. We measured 10 eggshell elements (As, Cd, Cr, Cu, Ni, Pb, Zn, Se, Sr, and Ca) and several shell characteristics (mass, thickness, porosity, and color). We found significant variation among populations in eggshell metal levels for all metals except copper. Eggshell lead, zinc, and chromium levels decreased from central Europe to the north, in line with the gradient in pollution levels over Europe, thus suggesting that eggshell can be used as an indicator of pollution levels. Eggshell lead levels were also correlated with soil lead levels and pH. Most of the metals were not correlated with eggshell characteristics, with the exception of shell mass, or with breeding success, which may suggest that birds can cope well with the current background exposure levels across Europe.
    https://doi.org/10.1007/s11356-013-2299-0
  • Proceedings of the Royal Society B-Biological Sciences
    2014

    Why climate change will invariably alter selection pressures on phenology

    Phillip Gienapp, Thomas Reed, Marcel E. Visser
    The seasonal timing of lifecycle events is closely linked to individual fitness and hence, maladaptation in phenological traits may impact population dynamics. However, few studies have analysed whether and why climate change will alter selection pressures and hence possibly induce maladaptation in phenology. To fill this gap, we here use a theoretical modelling approach. In our models, the phenologies of consumer and resource are (potentially) environmentally sensitive and depend on two different but correlated environmental variables. Fitness of the consumer depends on the phenological match with the resource. Because we explicitly model the dependence of the phenologies on environmental variables, we can test how differential (heterogeneous) versus equal (homogeneous) rates of change in the environmental variables affect selection on consumer phenology. As expected, under heterogeneous change, phenotypic plasticity is insufficient and thus selection on consumer phenology arises. However, even homogeneous change leads to directional selection on consumer phenology. This is because the consumer reaction norm has historically evolved to be flatter than the resource reaction norm, owing to time lags and imperfect cue reliability. Climate change will therefore lead to increased selection on consumer phenology across a broad range of situations.
    https://doi.org/10.1098/rspb.2014.1611
  • Heredity
    2014

    Replicated high-density genetic maps of two great tit populations reveal fine-scale genomic departures from sex-equal recombination rates

    Kees van Oers, A.W. Santure, I. de Cauwer, N.E.M. Van Bers, R.P.M.A. Crooijmans, Ben C. Sheldon, Marcel E. Visser, J. Slate, M.A.M. Groenen
    Linking variation in quantitative traits to variation in the genome is an important, but challenging task in the study of life-history evolution. Linkage maps provide a valuable tool for the unravelling of such trait−gene associations. Moreover, they give insight into recombination landscapes and between-species karyotype evolution. Here we used genotype data, generated from a 10k single-nucleotide polymorphism (SNP) chip, of over 2000 individuals to produce high-density linkage maps of the great tit (Parus major), a passerine bird that serves as a model species for ecological and evolutionary questions. We created independent maps from two distinct populations: a captive F2-cross from The Netherlands (NL) and a wild population from the United Kingdom (UK). The two maps contained 6554 SNPs in 32 linkage groups, spanning 2010 cM and 1917 cM for the NL and UK populations, respectively, and were similar in size and marker order. Subtle levels of heterochiasmy within and between chromosomes were remarkably consistent between the populations, suggesting that the local departures from sex-equal recombination rates have evolved. This key and surprising result would have been impossible to detect if only one population was mapped. A comparison with zebra finch Taeniopygia guttata, chicken Gallus gallus and the green anole lizard Anolis carolinensis genomes provided further insight into the evolution of avian karyotypes.
    https://doi.org/10.1038/hdy.2013.107
  • PLoS One
    2014

    Mate Preference of Female Blue Tits Varies with Experimental Photoperiod

    L.B. Reparaz, Kees van Oers, Marc Naguib, C. Doutrelant, Marcel E. Visser, Samuel P. Caro
    Organisms use environmental cues to time their life-cycles and among these cues, photoperiod is the main trigger of reproductive behaviours such as territory defence or song activity. Whether photoperiod is also important for another behaviour closely associated with reproduction, mate choice, is unknown. In many bird species, mate choice occurs at two different times during the annual cycle that strongly differ in daylength: in late winter when photoperiod is short and social mates are chosen, and again around egg-laying when photoperiod is longer and extra-pair mates are chosen. This duality makes the role that photoperiod plays on mate choice behaviours intriguing. We investigated the effect of photoperiod on mate choice using three experimental photoperiodic treatments (9 L:15 D, 14 L:10 D, 18 L:6 D), using blue tits (Cyanistes caeruleus) as a biological model. We show that female choice was stronger under long photoperiods. In addition, female blue tits spent significantly more time near males with long tarsi and long wings. This latter preference was only expressed under long photoperiods, suggesting that some indices of male quality only become significant to females when they are strongly photostimulated, and therefore that females could select their social and extra-pair mates based on different phenotypic traits. These results shed light on the roles that photoperiod may play in stimulating pair-bonding and in refining female selectivity for male traits.
    https://doi.org/10.1371/journal.pone.0092527
  • Ibis
    2014

    Longitudinal data reveal ontogenetic changes in the wing morphology of a long-distance migratory bird

    Iván De la Hera, F. Pulido, Marcel E. Visser
    In migratory bird species, juveniles normally have shorter and more rounded wings than adults. The causes of this age-specific difference in wing morphology, however, are largely unknown. Here, we used longitudinal data collected over 3 years from a Pied Flycatcher Ficedula hypoleuca population to assess whether age-related differences in wing morphology are a consequence of ontogenetic changes or of selection favouring birds with longer and more pointed wings. Our study provides evidence of ontogenetic changes in wing length and shape, whereby birds grow longer and more pointed wings as they grow older. Age-dependent variation is likely to be adaptive and may partly explain age differences in spring migration phenology and breeding success.
    https://doi.org/10.1111/ibi.12112
  • Journal of Evolutionary Biology
    2013

    Genetic background, and not ontogenetic effects, affect avian seasonal timing of reproduction

    Phillip Gienapp, Arie Van Noordwijk, Marcel E. Visser
    Avian seasonal timing is a life-history trait with important fitness consequences and which is currently under directional selection due to climate change. To predict micro-evolution in this trait, it is crucial to properly estimate its heritability. Heritabilities are often estimated from pedigreed wild populations. As these are observational data, it leaves the possibility that the resemblance between related individuals is not due to shared genes but to ontogenetic effects; when the environment for the offspring provided by early laying pairs differs from that by late pairs and the laying dates of these offspring when they reproduce themselves is affected by this environment, this may lead to inflated heritability estimates. Using simulation studies, we first tested whether and how much such an early environmental effect can inflate heritability estimates from animal models, and we showed that pedigree structure determines by how much early environmental effects inflate heritability estimates. We then used data from a wild population of great tits (Parus major) to compare laying dates of females born early in the season in first broods and from sisters born much later, in second broods. These birds are raised under very different environmental conditions but have the same genetic background. The laying dates of first and second brood offspring do not differ when they reproduce themselves, clearly showing that ontogenetic effects are very small and hence, family resemblance in timing is due to genes. This finding is essential for the interpretation of the heritabilities reported from wild populations and for predicting micro-evolution in response to climate change.
    https://doi.org/10.1111/jeb.12205
  • Journal of Animal Ecology
    2013

    Phenological mismatch strongly affects individual fitness but not population demography in a woodland passerine

    Thomas Reed, S. Jenouvrier, Marcel E. Visser
    Populations are shifting their phenology in response to climate change, but these shifts are often asynchronous among interacting species. Resulting phenological mismatches can drive simultaneous changes in natural selection and population demography, but the links between these interacting processes are poorly understood. Here we analyse 37 years of data from an individual-based study of great tits (Parus major) in the Netherlands and use mixed-effects models to separate the within- and across-year effects of phenological mismatch between great tits and caterpillars (a key food source for developing nestlings) on components of fitness at the individual and population levels. Several components of individual fitness were affected by individual mismatch (i.e. late breeding relative to the caterpillar food peak date), including the probability of double-brooding, fledgling success, offspring recruitment probability and the number of recruits. Together these effects contributed to an overall negative relationship between relative fitness and laying dates, that is, selection for earlier laying on average. Directional selection for earlier laying was stronger in years where birds bred on average later than the food peak, but was weak or absent in years where the phenology of birds and caterpillars matched (i.e. no population mismatch). The mean number of fledglings per female was lower in years when population mismatch was high, in part because fewer second broods were produced. Population mismatch had a weak effect on the mean number of recruits per female, and no effect on mean adult survival, after controlling for the effects of breeding density and the quality of the autumnal beech (Fagus sylvatica) crop. These findings illustrate how climate change-induced mismatch can have strong effects on the relative fitness of phenotypes within years, but weak effects on mean demographic rates across years. We discuss various general mechanisms that influence the extent of coupling between breeding phenology, selection and population dynamics in open populations subject to strong density regulation and stochasticity.
    https://doi.org/10.1111/j.1365-2656.2012.02020.x
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    2013

    Predicting demographically-sustainable rates of adaptation: can great tit breeding time keep pace with climate change?

    Phillip Gienapp, Marjolein Lof, Thomas Reed, J.M. McNamara, S. Verhulst, Marcel E. Visser
    Populations need to adapt to sustained climate change, which requires micro-evolutionary change in the long term. A key question is how the rate of this micro-evolutionary change compares with the rate of environmental change, given that theoretically there is a ‘critical rate of environmental change’ beyond which increased maladaptation leads to population extinction. Here, we parametrize two closely related models to predict this critical rate using data from a long-term study of great tits (Parus major). We used stochastic dynamic programming to predict changes in optimal breeding time under three different climate scenarios. Using these results we parametrized two theoretical models to predict critical rates. Results from both models agreed qualitatively in that even ‘mild’ rates of climate change would be close to these critical rates with respect to great tit breeding time, while for scenarios close to the upper limit of IPCC climate projections the calculated critical rates would be clearly exceeded with possible consequences for population persistence. We therefore tentatively conclude that micro-evolution, together with plasticity, would rescue only the population from mild rates of climate change, although the models make many simplifying assumptions that remain to be tested.
    https://doi.org/10.1098/rstb.2012.0289
  • Journal of Avian Biology
    2013

    Variation in eggshell traits between geographically distant populations of pied flycatchers Ficedula hypoleuca

    J. Morales, Suvi Ruuskanen, T. Laaksonen, R. Mateo, Eugen Belskii, T. Eeva, A. Jarvinen, A. Kerimov, E. Korpimaki, I. Krams, C. Morosinotto, R. Mand, M. Orell, A. Qvarnstrom, H. Siitari, F.M. Slager, V. Tiglar, Marcel E. Visser, W. Winkel, H. Zang, J. Moreno
    The expression and impact of maternal effects may vary greatly between populations and environments. However, little is known about large-scale geographical patterns of variation in maternal deposition to eggs. In birds, as in other oviparous animals, the outermost maternal component of an egg is the shell, which protects the embryo, provides essential mineral resources and allows its interaction with the environment in the form of gas exchange. In this study, we explored variation of eggshell traits (mass, thickness, pore density and pigmentation) across 15 pied flycatcher populations at a large geographic scale. We found significant between-population variation in all eggshell traits, except in pore density, suggesting spatial variation in their adaptive benefits or in the females’ physiological limitations during egg laying. Between- population variation in shell structure was not due to geographic location (latitude and longitude) or habitat type. However, eggshells were thicker in populations that experienced higher ambient temperature during egg laying. This could be a result of maternal resource allocation to the shell being constrained under low temperatures or of an adaptation to reduce egg water loss under high temperatures. We also found that eggshell colour intensity was positively associated with biliverdin pigment concentration, shell thickness and pore density. To conclude, our findings reveal large- scale between-population variation of eggshell traits, although we found little environmental dependency in their expression. Our findings call for further studies that explore other environmental factors (e.g. calcium availability and pollution levels) and social factors like sexual selection intensity that may account for differences in shell structure between populations.
    https://doi.org/10.1111/j.1600-048X.2012.05782.x
  • General and Comparative Endocrinology
    2013

    Is microevolution the only emergency exit in a warming world? Temperature influences egg laying but not its underlying mechanisms in great tits

    Samuel P. Caro, Sonja Schaper, A. Dawson, P. Sharp, Phillip Gienapp, Marcel E. Visser
    Many bird species have advanced their seasonal timing in response to global warming, but we still know little about the causal effect of temperature. We carried out experiments in climate-controlled aviaries to investigate how temperature affects luteinizing hormone, prolactin, gonadal development, timing of egg laying and onset of moult in male and female great tits. We used both natural and artificial temperature patterns to identify the temperature characteristics that matter for birds. Our results show that temperature has a direct, causal effect on onset of egg-laying, and in particular, that it is the pattern of increase rather than the absolute temperature that birds use. Surprisingly, the pre-breeding increases in plasma LH, prolactin and in gonadal size are not affected by increasing temperature, nor do they correlate with the onset of laying. This suggests that the decision to start breeding and its regulatory mechanisms are fine-tuned by different factors. We also found similarities between siblings in the timing of both the onset of reproduction and associated changes in plasma LH, prolactin and gonadal development. In conclusion, while temperature affects the timing of egg laying, the neuroendocrine system does not seem to be regulated by moderate temperature changes. This lack of responsiveness may restrain the advance in the timing of breeding in response to climate change. But as there is heritable genetic variation on which natural selection can act, microevolution can take place, and may represent the only way to adapt to a warming world.
    https://doi.org/10.1016/j.ygcen.2013.02.025
  • Journal of Avian Biology
    2013

    Great tits provided with ad libitum food lay larger eggs when exposed to colder temperatures

    Sonja Schaper, Marcel E. Visser
    The amount of nutrients deposited into a bird egg varies both between and within clutches of the same female. Larger eggs enhance offspring traits, but as a tradeoff, laying large eggs also infers energetic costs to the female. Income breeders usually lay larger eggs later in the season, when temperatures and food availability are higher. Egg size is thus affected by the daily amount of energy available to produce an egg under cold conditions, but it is less well known in how far temperature exerts direct effects on egg size. We show that great tit females Parus major with access to ad libitum food and breeding in climate-controlled aviaries varied their egg investments. The size of an individual egg was best predicted by mean temperatures one week pre-laying, with females laying larger, rather than smaller, eggs under colder conditions. Eggs increased in size over the season, but not significantly over the laying sequence. The degree of daily temperature fluctuation did not influence egg size. In addition to a substantial between-female variation, sisters were more similar to each other than unrelated females, showing that egg size does also reflect heritable intrinsic female properties. Natural variation in egg size is thus not only determined by energy-limitation, but also due to females allocating more resources to eggs laid in colder environments, thus increasing early survival of the chicks. That the positive correlation between temperature and egg investments that is found in a natural population is reversed under ad libitum food conditions demonstrates that wild great tits tradeoff own condition with survival prospects of their chicks as a function of available food, not ambient temperature.
    https://doi.org/10.1111/j.1600-048X.2012.00129.x
  • PLoS Biology
    2013

    The case of the missing mechanism: how does temperature influence seasonal timing in endotherms?

    Samuel P. Caro, Sonja Schaper, R.A. Hut, G.F. Ball, Marcel E. Visser
    Temperature has a strong effect on the seasonal timing of life-history stages in both mammals and birds, even though these species can regulate their body temperature under a wide range of ambient temperatures. Correlational studies showing this effect have recently been supported by experiments demonstrating a direct, causal relationship between ambient temperature and seasonal timing. Predicting how endotherms will respond to global warming requires an understanding of the physiological mechanisms by which temperature affects the seasonal timing of life histories. These mechanisms, however, remain obscure. We outline a road map for research aimed at identifying the pathways through which temperature is translated into seasonal timing.
    https://doi.org/10.1371/journal.pbio.1001517
  • Ecology Letters
    2013

    Birds exploit herbivore-induced plant volatiles to locate herbivorous prey

    Luisa Amo de Paz, Jeroen Jansen, Nicole M. van Dam, Marcel Dicke, Marcel E. Visser
    Arthropod herbivory induces plant volatiles that can be used by natural enemies of the herbivores to find their prey. This has been studied mainly for arthropods that prey upon or parasitise herbivorous arthropods but rarely for insectivorous birds, one of the main groups of predators of herbivorous insects such as lepidopteran larvae. Here, we show that great tits (Parus major) discriminate between caterpillar-infested and uninfested trees. Birds were attracted to infested trees, even when they could not see the larvae or their feeding damage. We furthermore show that infested and uninfested trees differ in volatile emissions and visual characteristics. Finally, we show, for the first time, that birds smell which tree is infested with their prey based on differences in volatile profiles emitted by infested and uninfested trees. Volatiles emitted by plants in response to herbivory by lepidopteran larvae thus not only attract predatory insects but also vertebrate predators.
    https://doi.org/10.1111/ele.12177
  • Journal of Evolutionary Biology
    2013

    Heritability of gonad size varies across season in a wild songbird

    Sonja Schaper, Phillip Gienapp, A. Dawson, Marcel E. Visser
    Many organisms advance their seasonal reproduction in response to global warming. In birds, which regress their gonads to a nonfunctional state each winter, these shifts are ultimately constrained by the time required for gonadal development in spring. Gonadal development is photoperiodically controlled and shows limited phenotypic plasticity in relation to environmental factors, such as temperature. Heritable variation in the time required for full gonadal maturation to be completed, based on both onset and speed of development and resulting in seasonally different gonad sizes among individuals, is thus a crucial prerequisite for an adaptive advancement of seasonal reproduction in response to changing temperatures. We measured seasonal gonadal development in climate-controlled aviaries for 144 great tit (Parus major) pairs, which consisted of siblings obtained as whole broods from the wild. We show that the extent of ovarian follicle development (follicle size) in early spring is highly heritable (h2 = 0.73) in females, but found no heritability of the extent of testis development in males. However, heritability in females decreased as spring advanced, caused by an increase in environmental variance and a decrease in additive genetic variation. This low heritability of the variation in a physiological mechanism underlying reproductive timing at the time of selection may hamper genetic adaptation to climate change, a key insight as this great tit population is currently under directional selection for advanced egg-laying.
    https://doi.org/10.1111/jeb.12249
  • Evolutionary Ecology
    2013

    Feather mass and winter moult extent are heritable but not associated with fitness-related traits in a long-distance migratory bird

    Iván De la Hera, Thomas Reed, F. Pulido, Marcel E. Visser
    In birds, the allocation of resources to plumage production may have important fitness consequences. However, we have only a limited understanding of how plumage traits respond to natural selection, making it difficult to predict how variation in plumage traits may contribute to the adaptation of birds to environmental change. In this study, we collected plumage-related data in a pedigreed population of a long-distance migratory bird (the Pied Flycatcher Ficedula hypoleuca) to estimate the heritability of two plumage traits: feather mass (as a proxy of feather quality) and the extent of winter moult. We further explored whether these plumage features were associated with some fitness-related traits. Variation in plumage characteristics could be explained by differences in sex, age and year, which indicates a high degree of plasticity in these traits. After controlling for these effects, however, feather mass and winter moult extent were highly repeatable (r = 0.58–0.82) and heritable (h2 = 0.59–0.65), suggesting that additive genetic variation accounts for a significant proportion of the residual phenotypic variation of plumage traits in this population. Although the studied characteristics showed evolutionary potential, we did not find any relationship between plumage features and fitness-related traits like spring arrival date, egg-laying date, mating success or mating-time. We conclude that current selection on feather mass and moult extent, if existing, is weak, and that these moult-related traits are currently of minor importance for the adaptation of our study population to global warming.
    https://doi.org/10.1007/s10682-013-9639-x
  • Science Magazine
    2013

    Population growth in a wild bird is buffered against phenological mismatch

    Thomas Reed, V. Grotan, S. Jenouvrier, Bernt-Erik Sæther, Marcel E. Visser
    road-scale environmental changes are altering patterns of natural selection in the wild, but few empirical studies have quantified the demographic cost of sustained directional selection in response to these changes. We tested whether population growth in a wild bird is negatively affected by climate change–induced phenological mismatch, using almost four decades of individual-level life-history data from a great tit population. In this population, warmer springs have generated a mismatch between the annual breeding time and the seasonal food peak, intensifying directional selection for earlier laying dates. Interannual variation in population mismatch has not, however, affected population growth. We demonstrated a mechanism contributing to this uncoupling, whereby fitness losses associated with mismatch are counteracted by fitness gains due to relaxed competition. These findings imply that natural populations may be able to tolerate considerable maladaptation driven by shifting climatic conditions without undergoing immediate declines.
    https://doi.org/10.1126/science.1232870
  • Nature Climate Change
    2013

    Evolutionary response of the egg hatching date of a herbivorous insect under climate change

    M. Van Asch, Lucia Salis, L.J.M. Holleman, Bart van Lith, Marcel E. Visser
    Under changing climatic conditions, species need to adapt to their new environment. Genetic adaptation is crucial to prevent population extinction1 but examples where climate change leads to genetic changes in wild populations have been few2, 3. The synchronization between the timing of egg hatching of a herbivorous insect, the winter moth (Operophtera brumata), and the seasonal bud burst of its food plant, oak (Quercus robur), has been disrupted by climate change4 and a quantitative genetic model predicts that selection will delay the egg hatching date5. Here we show, using both long-term observational data and experiments, that the egg hatching date has changed genetically, resulting in closer synchrony with oak bud burst. The observed rate of change matches the predicted rate of change of one day per year. Hence, altered selection pressures, caused by environmental change, result in a rapid adaptive response in insect phenology. These genetic changes in a key life-history trait in this herbivorous insect therefore seem to be fast enough to match the climate-change-induced advancement of their host phenology.
    https://doi.org/10.1038/NCLIMATE1717
  • General and Comparative Endocrinology
    2012

    Individual variation in avian reproductive physiology does not reliably predict variation in laying date

    Sonja Schaper, A. Dawson, P.J. Sharp, Samuel P. Caro, Marcel E. Visser
    Most animals reproduce seasonally. They time their reproduction in response to environmental cues, like increasing photoperiod and temperature, which are predictive for the time of high food availability. Although individuals of a population use the same cues, they vary in their onset of reproduction, with some animals reproducing consistently early or late. In avian research, timing of reproduction often refers to the laying date of the first egg, which is a key determinant of fitness. Experiments measuring temporal patterns of reproductive hormone concentrations or gonadal size under controlled conditions in response to a cue commonly assume that these proxies are indicative of the timing of egg laying. This assumption often remains untested, with few studies reporting both reproductive development and the onset of laying. We kept in total 144 pairs of great tits (Parus major) in separate climate-controlled aviaries over 4 years to correlate pre-breeding plasma luteinizing hormone (LH), prolactin (PRL) and gonadal growth with the timing of laying. Individuals varied consistently in hormone concentrations over spring, but this was not directly related to the timing of gonadal growth, nor with the laying date of the first egg. The timing of gonadal development in both sexes was similarly not correlated with the timing of laying. This demonstrates the female’s ability to adjust the onset of laying to environmental conditions irrespective of substantial differences in pre-laying development. We conclude that stages of reproductive development are regulated by different cues, and therefore egg laying dates need to be studied to measure the influences of environmental cues on timing of seasonal reproduction.
    https://doi.org/10.1016/j.ygcen.2012.07.021
  • Journal of Ornithology
    2012

    Adaptive phenological mismatches of birds and their food in a warming world

    Marcel E. Visser, Luc te Marvelde, Marjolein Lof
    Climate change has profound ecological effects in birds, with the clearest effect a shift in timing, or phenology, of avian reproduction. To assess the consequences of these shifts, we performed a literature search and compared the rates of phenological change in the reproduction of birds with that of the food for their offspring. While in some areas the rate of change of the birds and their food was similar, there were also areas where the birds’ shift lagged behind that of their food. In these cases, this will lead to a phenological mismatch, which will affect the fitness of the brood. There are two hypotheses explaining why climate change leads to mismatched reproduction: either the cues used no longer accurately predict the peak in food abundance (the cues hypothesis) or the fitness costs of egg production and/or incubation of laying early enough to match reproduction are substantial in early spring and are not compensated by the fitness benefits of a better matched reproduction (constraint hypothesis). In the latter case, the phenological mismatch is adaptive. We present a simple mathematical model to show that this may be the case if there are fitness costs of egg laying and/or incubation under cold conditions and if the temperatures that determine the peak in food abundance increase stronger than the temperatures affecting the costs of egg laying and incubation, as is the case in the Netherlands. Whether or not a phenological mismatch is adaptive has important consequences for natural selection acting on timing of reproduction. If the mismatch is not adaptive, timing of reproduction will be under direct natural selection, while, if the mismatch is adaptive, selection is likely to be on the costs of egg production, possibly on egg size or adult size. In all cases, a mismatch is expected to have negative population consequences and, especially when the mismatch is adaptive, these consequences cannot be reduced by a response to natural selection on timing directly. This makes experimental studies on laying date, which can determine whether the mismatch is adaptive, of crucial importance.
    https://doi.org/10.1007/s10336-011-0770-6
  • Nature Climate Change
    2012

    Biology: Birds and butterflies in climatic debt

    A European-wide analysis of changing species distributions shows that butterflies outrun birds in the race to move northwards in response to climate change, but that neither group keeps up with increasing temperatures.
    https://doi.org/10.1038/nclimate1387
  • Oecologia
    2012

    Energy expenditure during egg laying is equal for early and late breeding free-living female great tits

    Luc te Marvelde, S.L. Webber, H.A.J. Meijer, Marcel E. Visser
    In many bird populations, variation in the timing of reproduction exists but it is not obvious how this variation is maintained as timing has substantial fitness consequences. Daily energy expenditure (DEE) during the egg laying period increases with decreasing temperatures and thus perhaps only females that can produce eggs at low energetic cost will lay early in the season, at low temperatures. We tested whether late laying females have a higher daily energy expenditure during egg laying than early laying females in 43 great tits (Parus major), by comparing on the same day the DEE of early females late in their laying sequence with DEE of late females early in their egg laying sequence. We also validated the assumption that there are no within female differences in DEE within the egg laying sequence. We found a negative effect of temperature and a positive effect of female body mass on DEE but no evidence for differences in DEE between early and late laying females. However, costs incurred during egg laying may have carry-over effects later in the breeding cycle and if such carry-over effects differ for early and late laying females this could contribute to the maintenance of phenotypic variation in laying dates.
    https://doi.org/10.1007/s00442-011-2122-x
  • American Naturalist
    2012

    Increasing temperature, not mean temperature, is a cue for avian timing of reproduction

    Sonja Schaper, A. Dawson, P. Sharp, Phillip Gienapp, Samuel P. Caro, Marcel E. Visser
    Timing of reproduction in temperate-zone birds is strongly correlated with spring temperature, with an earlier onset of breeding in warmer years. Females adjust their timing of egg laying between years to be synchronized with local food sources and thereby optimize reproductive output. However, climate change currently disrupts the link between predictive environmental cues and spring phenology. To investigate direct effects of temperature on the decision to lay and its genetic basis, we used pairs of great tits (Parus major) with known ancestry and exposed them to simulated spring scenarios in climate-controlled aviaries. In each of three years, we exposed birds to different patterns of changing temperature. We varied the timing of a temperature change, the daily temperature amplitude, and the onset and speed of a seasonal temperature rise. We show that females fine-tune their laying in response to a seasonal increase in temperature, whereas mean temperature and daily temperature variation alone do not affect laying dates. Luteinizing hormone concentrations and gonadal growth in early spring were not influenced by temperature or temperature rise, possibly posing a constraint to an advancement of breeding. Similarities between sisters in their laying dates indicate genetic variation in cue sensitivity. These results refine our understanding of how changes in spring climate might affect the mismatch in avian timing and thereby population viability.
    https://doi.org/10.1086/663675
  • PLoS One
    2012

    Activity patterns during food provisioning are affected by artificial light in free living great tits (Parus major)

    Mieke Titulaer, Kamiel Spoelstra, Cynthia Lange, Marcel E. Visser
    Artificial light may have severe ecological consequences but there is limited experimental work to assess these consequences. We carried out an experimental study on a wild population of great tits (Parus major) to assess the impact of light pollution on daily activity patterns during the chick provisioning period. Pairs that were provided with a small light outside their nest box did not alter the onset, cessation or duration of their working day. There was however a clear effect of artificial light on the feeding rate in the second half of the nestling period: when provided with artificial light females increased their feeding rate when the nestlings were between 9 and 16 days old. Artificial light is hypothesised to have affected the perceived photoperiod of either the parents or the offspring which in turn led to increased parental care. This may have negative fitness consequences for the parents, and light pollution may thus create an ecological trap for breeding birds.
    https://doi.org/10.1371/journal.pone.0037377
  • Proceedings of the Royal Society B-Biological Sciences
    2012

    Timing in a fluctuating environment: environmental variability and asymmetric fitness curves can lead to adaptively mismatched avian reproduction

    Marjolein Lof, Thomas Reed, J.M. McNamara, Marcel E. Visser
    Adaptation in dynamic environments depends on the grain, magnitude and predictability of ecological fluctuations experienced within and across generations. Phenotypic plasticity is a well-studied mechanism in this regard, yet the potentially complex effects of stochastic environmental variation on optimal mean trait values are often overlooked. Using an optimality model inspired by timing of reproduction in great tits, we show that temporal variation affects not only optimal reaction norm slope, but also elevation. With increased environmental variation and an asymmetric relationship between fitness and breeding date, optimal timing shifts away from the side of the fitness curve with the steepest decline. In a relatively constant environment, the timing of the birds is matched with the seasonal food peak, but they become adaptively mismatched in environments with temporal variation in temperature whenever the fitness curve is asymmetric. Various processes affecting the survival of offspring and parents influence this asymmetry, which collectively determine the ‘safest’ strategy, i.e. whether females should breed before, on, or after the food peak in a variable environment. As climate change might affect the (co)variance of environmental variables as well as their averages, risk aversion may influence how species should shift their seasonal timing in a warming world.
    https://doi.org/10.1098/rspb.2012.0431
  • Annual Review of Chronopharmacology
    2012

    Effects of temperature on circadian clock and chronotype: an experimental study in a passerine bird

    M. Lehmann, Kamiel Spoelstra, Marcel E. Visser, B. Helm
    Daily schedules of many organisms, including birds, are thought to affect fitness. Timing in birds is based on circadian clocks that have a heritable period length, but fitness consequences for individuals in natural environments depend on the scheduling of entrained clocks. This chronotype, i.e., timing of an individual relative to a zeitgeber, results from interactions between the endogenous circadian clock and environmental factors, including light conditions and ambient temperature. To understand contributions of these factors to timing, we studied daily activity patterns of a captive songbird, the great tit (Parus major), under different temperature and light conditions. Birds were kept in a light (L)-dark (D) cycle (12.5 L:11.5 D) at either 8°C or 18°C with ad libitum access to food and water. We assessed chronotype and subsequently tested birds at the same temperature under constant dim light (LLdim) to determine period length of their circadian clock. Thermal conditions were then reversed so that period length was measured under both temperatures. We found that under constant dim light conditions individuals lengthened their free-running period at higher temperatures by 5.7 ± 2.1 min (p = .002). Under LD, birds kept at 18°C started activity later and terminated it much earlier in the day than those kept under 8°C. Overall, chronotype was slightly earlier under higher temperature, and duration of activity was shorter. Furthermore, individuals timed their activities consistently on different days under LD and over the two test series under LLdim (repeatability from .38 to .60). Surprisingly, period length and chronotype did not show the correlation that had been previously found in other avian species. Our study shows that body clocks of birds are precise and repeatable, but are, nonetheless, affected by ambient temperature.
    https://doi.org/10.3109/07420528.2012.707159
  • PLoS One
    2012

    Manipulation of life-history decisions using leptin in a wild passerine

    Luc te Marvelde, Marcel E. Visser
    Seasonal timing of reproduction and the number of clutches produced per season are two key avian life-history traits with major fitness consequences. Female condition may play an important role in these decisions. In mammals, body condition and leptin levels are correlated. In birds, the role of leptin remains unclear. We did two experiments where we implanted female great tits with a pellet releasing leptin evenly for 14 days, to manipulate their perceived body condition, or a placebo pellet. In the first experiment where females were implanted when feeding their first brood offspring we found, surprisingly, that placebo treated females were more likely to initiate a second brood compared to leptin treated females. Only one second brood fledged two chicks while five were deserted late in the incubation stage or when the first egg hatched. No difference was found in female or male return rate or in recruitment rate of fledglings of the first brood, possibly due to the desertion of the second broods. In our study population, where there is selection for early egg laying, earlier timing of reproduction might be hampered by food availability and thus nutritional state of the female before egg laying. We therefore implanted similar leptin pellets three weeks before the expected start of egg laying in an attempt to manipulate the laying dates of first clutches. However, leptin treated females did not initiate egg laying earlier compared to placebo treated females, suggesting that other variables than the perceived body condition play a major role in the timing of reproduction. Also, leptin treatment did not affect body mass, basal metabolic rate or feeding rates in captive females. Manipulating life history decisions using experimental protocols which do not alter individuals’ energy balance are crucial in understanding the trade-off between costs and benefits of life history decisions.
    https://doi.org/10.1371/journal.pone.0034090
  • Journal of Animal Ecology
    2012

    Climate change, breeding date and nestling diet: how temperature differentially affects seasonal changes in pied flycatcher diet depending on habitat variation

    C. Burger, Eugen Belskii, T. Eeva, T. Laaksonen, M. Mägi, R. Mänd, A. Qvarnström, T. Slagsvold, T. Veen, Marcel E. Visser, Karen L. Wiebe, C. Wiley, J. Wright, Christiaan Both
    1.Climate warming has led to shifts in the seasonal timing of species. These shifts can differ across trophic levels, and as a result, predator phenology can get out of synchrony with prey phenology. This can have major consequences for predators such as population declines owing to low reproductive success. However, such trophic interactions are likely to differ between habitats, resulting in differential susceptibility of populations to increases in spring temperatures. A mismatch between breeding phenology and food abundance might be mitigated by dietary changes, but few studies have investigated this phenomenon. Here, we present data on nestling diets of nine different populations of pied flycatchers Ficedula hypoleuca, across their breeding range. This species has been shown to adjust its breeding phenology to local climate change, but sometimes insufficiently relative to the phenology of their presumed major prey: Lepidoptera larvae. In spring, such larvae have a pronounced peak in oak habitats, but to a much lesser extent in coniferous and other deciduous habitats. 2.We found strong seasonal declines in the proportions of caterpillars in the diet only for oak habitats, and not for the other forest types. The seasonal decline in oak habitats was most strongly observed in warmer years, indicating that potential mismatches were stronger in warmer years. However, in coniferous and other habitats, no such effect of spring temperature was found. 3.Chicks reached somewhat higher weights in broods provided with higher proportions of caterpillars, supporting the notion that caterpillars are an important food source and that the temporal match with the caterpillar peak may represent an important component of reproductive success. 4.We suggest that pied flycatchers breeding in oak habitats have greater need to adjust timing of breeding to rising spring temperatures, because of the strong seasonality in their food. Such between-habitat differences can have important consequences for population dynamics and should be taken into account in studies on phenotypic plasticity and adaptation to climate change.
    https://doi.org/10.1111/j.1365-2656.2012.01968.x
  • PLoS One
    2012

    A single long day triggers follicle growth in captive female Great Tits (Parus major) in winter but does not affect laying dates in the wild in spring

    Luc te Marvelde, Sonja Schaper, Marcel E. Visser
    In many forest passerine bird species, rapid climate warming has led to a phenological mismatch between the period of maximum nestlings' food requirements and the period of maximum food availability (seasonal caterpillar biomass peak) due to an insufficient advancement of the birds' laying dates. The initiation of laying is preceded by the development of the gonads, which in birds are regressed outside the breeding season. Increasing day length in late winter and early spring triggers a cascade of hormones which induces gonadal development. Since day length is not altered by climate change, one potential restriction to advancing laying date is the seasonal timing of gonadal development. To assess the importance of gonadal growth for timing of reproduction we experimentally manipulated the timing of gonadal development. We show that the growth of the largest follicle of captive female great tits (Parus major) increased after being exposed to just a single long day in winter (20 hours of light followed by 4 hours darkness). We then photostimulated wild female great tits from two study areas in a field experiment in spring for a single day and determined their laying date. These populations differed in the availability of food allowing us to test if food availability in combination with photostimulation affected egg laying dates. Despite an expected difference in the onset of gonadal growth, laying dates of photostimulated females did not differ from control females in both populations. These results suggest that wild great tits are not restricted in the advancement of their laying date by limited gonadal development.
    https://doi.org/10.1371/journal.pone.0035617
  • Molecular Ecology Resources
    2012

    The design and cross-population application of a genome-wide SNP chip for the great tit Parus major

    N.E.M. Van Bers, A.W. Santure, Kees van Oers, I. de Cauwer, Bert W. Dibbits, A.C. Mateman, R.P.M.A. Crooijmans, Ben C. Sheldon, Marcel E. Visser, M.A.M. Groenen, J. Slate
    The vast amount of phenotypic information collected in some wild animal populations makes them extremely valuable for unravelling the genetics of ecologically important traits and understanding how populations adapt to changes in their environment. Next generation sequencing has revolutionized the development of large marker panels in species previously lacking genomic resources. In this study, a unique genomics toolkit was developed for the great tit (Parus major), a model species in ecology and behavioural biology. This toolkit consists of nearly 100 000 SNPs, over 250 million nucleotides of assembled genomic DNA and more than 80 million nucleotides of assembled expressed sequences. A SNP chip with 9193 SNP markers expected to be spaced evenly along the great tit genome was used to genotype 4702 birds from two of the most intensively studied natural vertebrate populations [Wytham Woods/Bagley Woods (United Kingdom) and de Hoge Veluwe/Westerheide (The Netherlands)]. We show that (i) SNPs identified in either of the two populations have a high genotyping success in the other population, (ii) the minor allele frequencies of the SNPs are highly correlated between the two populations and (iii) despite this high correlation, a large number of SNPs display significant differentiation (FST) between the populations, with an overrepresentation of genes involved in cardiovascular development close to these SNPs. The developed resources provide the basis for unravelling the genetics of important traits in many long-term studies of great tits. More generally, the protocols and pitfalls encountered will be of use for those developing similar resources.
    https://doi.org/10.1111/j.1755-0998.2012.03141.x
  • Functional Ecology
    2011

    Mismatched reproduction is energetically costly for chick feeding female great tits

    Luc te Marvelde, S.L. Webber, H.A.J. Meijer, Marcel E. Visser
    1. Climate change has caused a phenological mismatch between the timing of reproduction and the local food peak in many bird species. Late breeding birds therefore experience reduced food availability during chick rearing and are thus predicted to have an increased energy expenditure. Observational studies, however, show mixed results, perhaps because they compare energy expenditure across rather than within individuals at different levels of food availability. 2. In a cross foster experiment, we measured daily energy expenditure (DEE) twice within individuals during chick feeding (when chicks were 6 and 14 days old) for 28 free-living female great tits (Parus major). To avoid confounding effects of chick age, these females reared on both occasions a standardized foster brood of eight 10-day-old chicks during the 24-h measuring period. For all birds, food availability declined between the two measurements. 3. We show that DEE during chick feeding increased within females when food availability decreased. Variation in DEE within females is partly explained by brood visit rates, food availability and temperature. 4. DEE during chick feeding could be affected by the investment in previous stages of the reproductive attempt. However, energy expenditure during chick feeding was not correlated to energy expenditure during egg laying, measured in these same females. 5. Understanding of energetic costs during all phases of the reproductive cycle is important to forecast the consequences of climate warming on timing of reproduction.
    https://doi.org/10.1111/j.1365-2435.2011.01889.x
  • PLoS One
    2011

    Sleeping birds do not respond to predator odour

    Luisa Amo de Paz, Samuel P. Caro, Marcel E. Visser
    Background: During sleep animals are relatively unresponsive and unaware of their environment, and therefore, more exposed to predation risk than alert and awake animals. This vulnerability might influence when, where and how animals sleep depending on the risk of predation perceived before going to sleep. Less clear is whether animals remain sensitive to predation cues when already asleep. Methodology/Principal Findings: We experimentally tested whether great tits are able to detect the chemical cues of a common nocturnal predator while sleeping. We predicted that birds exposed to the scent of a mammalian predator (mustelid) twice during the night would not go into torpor (which reduces their vigilance) and hence would not reduce their body temperature as much as control birds, exposed to the scent of another mammal that does not represent a danger for the birds (rabbit). As a consequence of the higher body temperature birds exposed to the scent of a predator are predicted to have a higher resting metabolic rate (RMR) and to lose more body mass. In the experiment, all birds decreased their body temperature during the night, but we did not find any influence of the treatment on body temperature, RMR, or body mass. Conclusions/Significance: Our results suggest that birds are not able to detect predator chemical cues while sleeping. As a consequence, antipredatory strategies taken before sleep, such as roosting sites inspection, may be crucial to cope with the vulnerability to predation risk while sleeping.
    https://doi.org/10.1371/journal.pone.0027576
  • Journal of Field Ornithology
    2011

    A new method for catching cavity-nesting birds during egg laying and incubation

    Luc te Marvelde, S.L. Webber, AB. Van den Burg, Marcel E. Visser
    The physiological condition of female birds during the egg-laying and incubation periods is of considerable interest and yet is relatively understudied in wild birds, primarily due to the difficulty of catching birds during this period without causing nest desertion. We therefore developed a box-net to capture cavity-nesting birds using sections of a mist-net placed around a metal cubic frame. We captured female Great Tits (Parus major) as they left nest boxes during the egg-laying and incubation periods and measured desertion rates. Using box-nets, we captured 108 of 119 (90%) females during egg laying and 10 of 12 (83%) during incubation. Our recapture rate over two consecutive days during incubation was 50% (5 of 10). Females not captured left nest boxes before we attempted to capture them, escaped through a hole in the mist-net, or remained in nest boxes for more than 2 h, after which we ended capture attempts. Overall, 22% of egg-laying females deserted, with desertion rates highest early in the egg-laying period. Desertion rates of females captured using box-nets did not differ from those of undisturbed females. One of 10 females captured in a box-net deserted during the incubation period. Box-nets are portable, can be set up and taken down quickly and easily, and could potentially be used with nest boxes or natural cavities at any height. Box-nets are easy to construct and adaptable for use with an array of cavity-nesting birds, and can be an important tool for studying female physiology during egg laying and incubation.
    https://doi.org/10.1111/j.1557-9263.2011.00335.x
  • Journal of Insect Conservation
    2011

    Synchronisation of egg hatching of brown hairstreak (Thecla betulae) and budburst of blackthorn (Prunus spinosa) in a warmer future

    H.H. De Vries, S.H. Ens, G. de Graaf, L. Teunissen, R. te Velde, L. Vogelaar, A. Winterink, Marcel E. Visser
    Synchronisation of the phenology of insect herbivores and their larval food plant is essential for the herbivores’ fitness. The monophagous brown hairstreak (Thecla betulae) lays its eggs during summer, hibernates as an egg, and hatches in April or May in the Netherlands. Its main larval food plant blackthorn (Prunus spinosa) flowers in early spring, just before the leaves appear. As soon as the Blackthorn opens its buds, and this varies with spring temperatures, food becomes available for the brown hairstreak. However, the suitability of the leaves as food for the young caterpillars is expected to decrease rapidly. Therefore, the timing of egg hatch is an important factor for larval growth. This study evaluates food availability for brown hairstreak at different temperatures. Egg hatch and budburst were monitored from 2004 to 2008 at different sites in the Netherlands. Results showed ample food availability at all monitored temperatures and sites but the degree of synchrony varied strongly with spring temperatures. To further study the effect of temperature on synchronisation, an experiment using normal temperatures of a reference year (T) and temperatures of T + 5°C was carried out in climate chambers. At T + 5°C, both budburst and egg hatch took place about 20 days earlier and thus, on average, elevated temperature did not affect synchrony. However, the total period of budburst was 11 days longer, whereas the period of egg hatching was 3 days shorter. The implications for larval growth by the brown hairstreak under a warmer climate are considered.
    https://doi.org/10.1007/s10841-010-9355-6
  • American Naturalist
    2011

    Testing mechanisms of Bergmann’s rule: Phenotypic decline but no genetic change in body size in three posserine bird populations

    A. Husby, S.M. Hille, Marcel E. Visser
    Bergmann’s rule predicts a decrease in body size with increasing temperature and has much empirical support. Surprisingly, we know very little about whether “Bergmann size clines” are due to a genetic response or are a consequence of phenotypic plasticity. Here, we use data on body size (mass and tarsus length) from three long-term (1979–2008) study populations of great tits (Parus major) that experienced a temperature increase to examine mechanisms behind Bergmann’s rule. We show that adult body mass decreased over the study period in all populations and that tarsus length increased in one population. Both body mass and tarsus length were heritable and under weak positive directional selection, predicting an increase, rather than a decrease, in body mass. There was no support for microevolutionary change, and thus the observed declines in body mass were likely a result of phenotypic plasticity. Interestingly, this plasticity was not in direct response to temperature changes but seemed to be due to changes in prey dynamics. Our results caution against interpreting recent phenotypic body size declines as adaptive evolutionary responses to temperature changes and highlight the importance of considering alternative environmental factors when testing size clines.
    https://doi.org/10.1086/660834
  • Functional Ecology
    2011

    Genetic variation in cue sensitivity involved in avian timing of reproduction

    Marcel E. Visser, Sonja Schaper, L.J.M. Holleman, A. Dawson, P. Sharp, Phillip Gienapp, Samuel P. Caro
    1.Annual variation in the timing of avian reproduction is associated with predictive cues related to ambient temperature. Understanding how these cues affect timing, and estimating the genetic variation in sensitivity to these cues, is essential to predict the micro-evolutionary changes in timing which are needed to adapt to climate change. 2.We carried out a 2-year experiment with great tits Parus major of known genetic background, which were kept in pairs in climate-controlled aviaries with simulated natural photoperiod and exposed to a seasonal change in temperature, where the two treatments differed by 4 °C. We recorded the dates of laying the first and last eggs and timing of moult, as well as physiological proxies associated with reproduction: plasma luteinizing hormone (LH), prolactin, and gonadal size at four-weekly intervals. 3.The temperature treatments did not affect first-egg dates, nor gonadal growth or plasma LH and prolactin concentrations. However, birds terminated egg laying, regressed their testes and started their moult earlier at higher temperatures. 4.There were marked family differences in both the start of egg laying, with sisters from early laying maternal families laying early, and in the termination of laying, indicating that there is heritable variation in sensitivity to cues involved in timing. 5.Our experiment, the first to use genetically related individuals in an experimental design with a natural change in photoperiod and biologically realistic temperature differences, thus shows that genetic adaptation in cue sensitivity is possible, essential for species to be able to adapt to a warming world.
    https://doi.org/10.1111/j.1365-2435.2011.01844.x
  • Ardea
    2011

    Smelling out predators is innate in birds

    Luisa Amo de Paz, Marcel E. Visser, Kees van Oers
    The role of olfaction for predation risk assessment remains barely explored in birds, although predator chemical cues could be useful in predator detection under low visibility conditions for many bird species. We examine whether Great Tits Parus major are able to use the odour of mustelids to assess predation risk when selecting cavities for roosting. We analysed whether the response to predator chemical cues is innate and assessed whether the antipredatory response is associated with exploratory behaviour, a proxy for the personality of birds. In a choice experiment in aviaries, we offered naïve adult Great Tits of known personality two nest-boxes, one control and one experimental. The experimental nest-box had the odour of a mustelid predator or a strong new odour without biological significance, the control nest-box contained no odour. When one of the cavities contained the odour of a predator, birds avoided the use of either of the two offered nest-boxes, whereas there was no avoidance of boxes when one of the nest-boxes contained a control odour. There was no relationship with exploratory behaviour. We show that the ability to use the chemical cues of predators is innate in birds, but individual differences in the response to predator chemical cues cannot be explained by the personality of the bird.
    https://doi.org/10.5253/078.099.0207
  • International Journal of Biometeorology
    2011

    Climate change, phenological shifts, eco-evolutionary responses and population viability: toward a unifying predictive approach

    S. Jenouvrier, Marcel E. Visser
    The debate on emission targets of greenhouse gasses designed to limit global climate change has to take into account the ecological consequences. One of the clearest ecological consequences is shifts in phenology. Linking these shifts to changes in population viability under various greenhouse gasses emission scenarios requires a unifying framework. We propose a box-in-a-box modeling approach that couples population models to phenological change. This approach unifies population modeling with both ecological responses to climate change as well as evolutionary processes. We advocate a mechanistic embedded correlative approach, where the link from genes to population is established using a periodic matrix population model. This periodic model has several major advantages: (1) it can include complex seasonal behaviors allowing an easy link with phenological shifts; (2) it provides the structure of the population at each phase, including the distribution of genotypes and phenotypes, allowing a link with evolutionary processes; and (3) it can incorporate the effect of climate at different time periods. We believe that the way climatologists have approached the problem, using atmosphere–ocean coupled circulation models in which components are gradually included and linked to each other, can provide a valuable example to ecologists. We hope that ecologists will take up this challenge and that our preliminary modeling framework will stimulate research toward a unifying predictive model of the ecological consequences of climate change.
    https://doi.org/10.1007/s00484-011-0458-x
  • PLoS Biology
    2011

    Speeding up microevolution: the effects of increasing temperature on selection and genetic variance in a wild bird population

    A. Husby, Marcel E. Visser, L.E.B. Kruuk
    The amount of genetic variance underlying a phenotypic trait and the strength of selection acting on that trait are two key parameters that determine any evolutionary response to selection. Despite substantial evidence that, in natural populations, both parameters may vary across environmental conditions, very little is known about the extent to which they may covary in response to environmental heterogeneity. Here we show that, in a wild population of great tits (Parus major), the strength of the directional selection gradients on timing of breeding increased with increasing spring temperatures, and that genotype-by-environment interactions also predicted an increase in additive genetic variance, and heritability, of timing of breeding with increasing spring temperature. Consequently, we therefore tested for an association between the annual selection gradients and levels of additive genetic variance expressed each year; this association was positive, but non-significant. However, there was a significant positive association between the annual selection differentials and the corresponding heritability. Such associations could potentially speed up the rate of micro-evolution and offer a largely ignored mechanism by which natural populations may adapt to environmental changes.
    https://doi.org/10.1371/journal.pbio.1000585
  • PLoS One
    2011

    Geographical variation in egg mass and egg content in a passerine bird

    Suvi Ruuskanen, H. Siitari, T. Eeva, Eugen Belskii, A. Järvinen, A. Kerimov, I. Krams, J. Moreno, C. Morosinotto, R. Mänd, E. Möstl, M. Orell, A. Qvarnström, J.P. Salminen, F.M. Slater, V. Tilgar, Marcel E. Visser, W. Winkel, H. Zang, T. Laaksonen
    Reproductive, phenotypic and life-history traits in many animal and plant taxa show geographic variation, indicating spatial variation in selection regimes. Maternal deposition to avian eggs, such as hormones, antibodies and antioxidants, critically affect development of the offspring, with long-lasting effects on the phenotype and fitness. Little is however known about large-scale geographical patterns of variation in maternal deposition to eggs. We studied geographical variation in egg components of a passerine bird, the pied flycatcher (Ficedula hypoleuca), by collecting samples from 16 populations and measuring egg and yolk mass, albumen lysozyme activity, yolk immunoglobulins, yolk androgens and yolk total carotenoids. We found significant variation among populations in most egg components, but ca. 90% of the variation was among individuals within populations. Population however explained 40% of the variation in carotenoid levels. In contrast to our hypothesis, we found geographical trends only in carotenoids, but not in any of the other egg components. Our results thus suggest high within-population variation and leave little scope for local adaptation and genetic differentiation in deposition of different egg components. The role of these maternally-derived resources in evolutionary change should be further investigated.
    https://doi.org/10.1371/journal.pone.0025360
  • Journal of Experimental Biology
    2011

    Spring phenology does not affect timing of reproduction in the great tit (Parus major)

    Sonja Schaper, C. Rueda, P.J. Sharp, A. Dawson, Marcel E. Visser
    Many seasonal breeders adjust the timing of reproduction in response to year-to-year variations in supplementary environmental cues, amongst which ambient temperature is thought to be most influential. However, it is possible that for species such as the great tit (Parus major L.), phenological cues from sprouting vegetation and the consequent abundance of invertebrate prey, although dependent on temperature, may provide supplementary environmental cues per se. This hypothesis was investigated in breeding pairs of great tits kept in outdoor aviaries. In spring, experimental pairs were provided with access to leafing birch branches and caterpillars as a visual food cue, while control pairs were provided with non-leafing branches. Observations were made on the onset of laying and on concentrations of plasma luteinizing hormone (LH) at regular intervals to monitor changes in reproductive function. The onset of egg laying was not advanced by the presence of leafing branches and caterpillars. LH concentrations increased during the course of the study, but phenological cues did not affect plasma LH levels in females and males. Early spring vegetation, such as the leafing of birch branches, and the appearance of caterpillar prey do not appear to play a significant role in fine-tuning the onset of egg laying in great tits.
    https://doi.org/10.1242/jeb.059543
  • Oecologia
    2011

    Geographical trends in the yolk carotenoid composition of the pied flycatcher (Ficedula hypoleuca)

    T. Eeva, Suvi Ruuskanen, J.P. Salminen, Eugen Belskii, A. Jarvinen, A. Kerimov, E. Korpimäki, I. Krams, J. Moreno, C. Morosinotto, R. Mänd, M. Orell, A. Qvarnström, H. Siitari, F.M. Slater, V. Tilgar, Marcel E. Visser, W. Winkel, H. Zang, T. Laaksonen
    Carotenoids in the egg yolks of birds are considered to be important antioxidants and immune stimulants during the rapid growth of embryos. Yolk carotenoid composition is strongly affected by the carotenoid composition of the female’s diet at the time of egg formation. Spatial and temporal differences in carotenoid availability may thus be reflected in yolk concentrations. To assess whether yolk carotenoid concentrations or carotenoid profiles show any large-scale geographical trends or differences among habitats, we collected yolk samples from 16 European populations of the pied flycatcher, Ficedula hypoleuca.Wefound that the concentrations and proportions of lutein and some other xanthophylls in the egg yolks decreased from Central Europe northwards. The most southern population (which is also the one found at the highest altitude) also showed relatively low carotenoid levels. Concentrations of b-carotene and zeaxanthin did not show any obvious geographical gradients. Egg yolks also contained proportionally more lutein and other xanthophylls in deciduous than in mixed or coniferous habitats. We suggest that latitudinal gradients in lutein and xanthophylls reflect the lower availability of lutein-rich food items in the northern F. hypoleuca populations and in montane southern populations, which start egg-laying earlier relative to tree phenology than the Central European populations. Similarly, among-habitat variation is likely to reflect the better availability of lutein-rich food in deciduous forests. Our study is the first to indicate that the concentration and profile of yolk carotenoids may show large-scale spatial variation among populations in different parts of the species’ geographical range. Further studies are needed to test the fitness effects of this geographical variation.
    https://doi.org/10.1007/s00442-010-1772-4
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    2010

    Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels

    Current predictions on species responses to climate change strongly rely on projecting altered environmental conditions on species distributions. However, it is increasingly acknowledged that climate change also influences species interactions. We review and synthesize literature information on biotic interactions and use it to argue that the abundance of species and the direction of selection during climate change vary depending on how their trophic interactions become disrupted. Plant abundance can be controlled by aboveground and belowground multitrophic level interactions with herbivores, pathogens, symbionts and their enemies. We discuss how these interactions may alter during climate change and the resulting species range shifts. We suggest conceptual analogies between species responses to climate warming and exotic species introduced in new ranges. There are also important differences: the herbivores, pathogens and mutualistic symbionts of range-expanding species and their enemies may co-migrate, and the continuous gene flow under climate warming can make adaptation in the expansion zone of range expanders different from that of cross-continental exotic species. We conclude that under climate change, results of altered species interactions may vary, ranging from species becoming rare to disproportionately abundant. Taking these possibilities into account will provide a new perspective on predicting species distribution under climate change.
    https://doi.org/10.1098/rstb.2010.0037
  • Evolution
    2010

    Contrasting patterns of phenotypic plasticity in reproductive traits in two great tit (Parus Major) populations

    A. Husby, D.H. Nussey, Marcel E. Visser, Alastair J Wilson, Ben C. Sheldon, L.E.B. Kruuk
    Phenotypic plasticity is an important mechanism via which populations can respond to changing environmental conditions, but we know very little about how natural populations vary with respect to plasticity. Here we use random-regression animal models to understand the multivariate phenotypic and genetic patterns of plasticity variation in two key life-history traits, laying date and clutch size, using data from long-term studies of great tits in The Netherlands (Hoge Veluwe [HV]) and UK (Wytham Woods [WW]). We show that, while population-level responses of laying date and clutch size to temperature were similar in the two populations, between-individual variation in plasticity differed markedly. Both populations showed significant variation in phenotypic plasticity (IxE) for laying date, but IxE was significantly higher in HV than in WW. There were no significant genotype-by-environment interactions (GxE) for laying date, yet differences in GxE were marginally nonsignificant between HV and WW. For clutch size, we only found significant IxE and GxE in WW but no significant difference between populations. From a multivariate perspective, plasticity in laying date was not correlated with plasticity in clutch size in either population. Our results suggest that generalizations about the form and cause of any response to changing environmental conditions across populations may be difficult.
    https://doi.org/10.1111/j.1558-5646.2010.00991.x
  • Journal of Avian Biology
    2010

    Similar patterns of age-specific reproduction in an island and mainland population of great tits Parus major

    Sandra Bouwhuis, Arie Van Noordwijk, Ben C. Sheldon, S. Verhulst, Marcel E. Visser
    The process of ageing was long thought to be too infrequent to affect life-histories in natural populations. Long-term studies have, however, recently demonstrated ageing to be ubiquitous even in the wild, although confounding factors, such as emigration instead of mortality, or inter-population variation in rates of ageing have seldom been addressed. Here, we present analyses of female age-specific reproductive performance in a Dutch island population of great tits Parus major. For this population with limited connectivity to surrounding areas, we show that, between individuals, reproductive lifespan positively co-varies with recruit production, while within individuals performance improves up to 3 years of age, after which it gradually declines. We also show these patterns to be strikingly similar to those recently found in a less isolated British mainland population of great tits, characterised by different environmental conditions and life-history strategies, in particular the frequency of multiple breeding. Our results therefore suggest patterns of agespecific reproductive performance to be robust to both environmental and life-history variation.
    https://doi.org/10.1111/j.1600-048X.2010.05111.x
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    2010

    Phenology, seasonal timing and circannual rhythms: towards a unified framework

    Marcel E. Visser, Samuel P. Caro, Kees van Oers, Sonja Schaper, B. Helm
    Phenology refers to the periodic appearance of life-cycle events and currently receives abundant attention as the effects of global change on phenology are so apparent. Phenology as a discipline observes these events and relates their annual variation to variation in climate. But phenology is also studied in other disciplines, each with their own perspective. Evolutionary ecologists study variation in seasonal timing and its fitness consequences, whereas chronobiologists emphasize the periodic nature of life-cycle stages and their underlying timing programmes (e.g. circannual rhythms). The (neuro-) endocrine processes underlying these life-cycle events are studied by physiologists and need to be linked to genes that are explored by molecular geneticists. In order to fully understand variation in phenology, we need to integrate these different perspectives, in particular by combining evolutionary and mechanistic approaches. We use avian research to characterize different perspectives and to highlight integration that has already been achieved. Building on this work, we outline a route towards uniting the different disciplines in a single framework, which may be used to better understand and, more importantly, to forecast climate change impacts on phenology.
    https://doi.org/10.1098/rstb.2010.0111
  • Ethology
    2010

    Singing activity reveals personality traits in great tits

    Marc Naguib, A.M. Kazek, Sonja Schaper, Kees van Oers, Marcel E. Visser
    In animal communication, sexually selected signals have been shown to often signal individual attributes such as motivation or quality. Birdsong is among the best studied signalling systems, and song traits vary substantially among individuals. The question remains if variation in signalling also reflects more general and consistent individual characteristics. Such consistent individual differences in behaviour that are relatively stable over time and contexts are referred to as personality or behavioural syndromes. Here, we studied the relation between singing and explorative behaviour, a well-studied personality trait, using great tits (Parus major) under standardized aviary conditions. The results show that singing activity measured as the number of songs sung in spring prior to breeding correlated with male but not with female explorative behaviour. In contrast, song repertoire was not related to explorative behaviour but varied over the day. The link between explorative and singing behaviour suggests that sexually selected signals are more than signals of quality but can also reflect other intrinsic behavioural characteristics such as personality traits.
    https://doi.org/10.1111/j.1439-0310.2010.01791.x
  • Ardea
    2010

    Across and within-forest effects on breeding success in Mediterranean Great Tits Parus major

    F. Atiénzar, Marcel E. Visser, J.L. Greño, L.J.M. Holleman, E.J. Belda, E. Barba
    Forest type and habitat structure can have profound effects on different aspects of avian life histories. These effects may, however, strongly differ across and within forests that vary in vegetation composition and structure, especially when an ancient forest has been replaced by a new forest. To test for these differences in effect, we studied Great Tit Parus major life-history traits (280 first clutches) in two Mediterranean evergreen forests during 2005–07: an ancient Holm Oak Quercus ilex and a reforested pine forest. A comparison between forests revealed that females breeding in the Holm Oak forest started laying one week later, and produced larger clutches and broods both at hatching and at fledging. Chicks raised in the Holm Oak forest also fledged in better condition. Within forests, however, the reproductive success was not higher for pairs breeding in nestboxes surrounded by oaks within the pine forest, and also reproductive success was not lower in nestboxes surrounded by pines within oak forest. Instead, vegetation maturity around nestboxes, rather than tree species composition, affected hatching success. Surprisingly, hatching success was higher in nestboxes surrounded by immature vegetation. We suggest that this may be due to a lower nest predation rate in nestboxes surrounded by immature vegetation, compared to nestboxes surrounded by mature vegetation. We suggest that different factors appear to affect variation in breeding success in Mediterranean Great Tits comparing across forests (e.g. food availability) vs. within a forest (e.g. nest predation).
    https://doi.org/10.5253/078.098.0110
  • Proceedings of the Royal Society B-Biological Sciences
    2010

    Heritable circadian period length in a wild bird population

    B. Helm, Marcel E. Visser
    Timing is essential, but circadian clocks, which play a crucial role in timekeeping, are almost unaddressed in evolutionary ecology. A key property of circadian clocks is their free-running period length (τ), i.e. the time taken for a full cycle under constant conditions. Under laboratory conditions, concordance of τ with the ambient light–dark cycle confers major fitness benefits, but little is known about period length and its implications in natural populations. We therefore studied natural variation of circadian traits in a songbird, the great tit (Parus major), by recording locomotor activity of 98 hand-raised, wild-derived individuals. We found, unexpectedly, that the free-running period of this diurnal species was significantly shorter than 24 h in constant dim light. We furthermore demonstrate, to our knowledge for the first time in a wild vertebrate, ample genetic variation and high heritability (h2 = 0.86 ± 0.24), implying that period length is potentially malleable by micro-evolutionary change. The observed, short period length may be a consequence of sexual selection, as offspring from extra-pair matings had significantly shorter free-running periods than their half-siblings from within-pair matings. These findings position circadian clocks in the ‘real world’ and underscore the value of using chronobiological approaches in evolutionary ecology. Evolutionary ecologists study variation and its fitness consequences, but often have difficulties relating behavioural variation to physiological mechanisms. The findings presented here open the possibility that properties of internal, circadian clocks affect performance in traits that are relevant to fitness and sexual selection.
    https://doi.org/10.1098/rspb.2010.0871
  • Functional Ecology
    2010

    Maternal effects in an insect herbivore as a mechanism to adapt to host plant phenology

    M. Van Asch, R. Julkunen-Tiito, Marcel E. Visser
    1.Maternal effects may play an important role in shaping the life history of organisms. Using an insect herbivore, the winter moth (Operophtera brumata) feeding on oak (Quercus robur), we show that maternal effects can affect seasonal timing of egg hatching in an herbivore in an adaptive way. 2. Winter moth egg-hatching needs to coincide with oak bud opening, as only freshly emerged leaves are suitable as food for the caterpillars. However, there is spatial variation in the timing of bud opening among oaks to which the winter moth needs to adapt. 3. We show experimentally that the generation time between the mother’s and her offsprings’ hatching dates was shorter for mothers who hatched late relative to bud opening of the tree they had to feed on (and hence had to feed on older leaves) than for mothers’ who hatched on time. Maternal feeding conditions affected both the larval and the pupal development time of the mother as well as the egg development time of her offspring: at all three stages developmental time was shorter for the mistimed treatment. 4.We thus show that adaptation to spatial variation may be achieved via maternal effects. While this is a mechanism selected to adapt to spatial variation, it may now also play a role in adaptation to climate change induced shifts in host phenology, and allow insect herbivores to adapt to changes in the seasonal timing of their food availability without the need for genetic change.
    https://doi.org/10.1111/j.1365-2435.2010.01734.x
  • Oecologia
    2010

    Temporal differences in food abundance promote coexistence between two congeneric passerines

    T. Veen, Ben C. Sheldon, F.J. Weissing, Marcel E. Visser, A. Qvarnström, G.-P. Sætre
    Many related species share the same environment and utilize similar resources. This is surprising because based on the principle of competitive exclusion one would predict that the superior competitor would drive the other species to extinction; coexistence is only predicted if interspecific competition is weaker than intraspecific competition. Interspecific competition is frequently reduced by differential resource use, resulting in habitat segregation. In this paper, we use the closely related collared and pied flycatcher to assess the potential of habitat differences to affect interspecific competition through a different mechanism, namely by generating temporal differences in availability of similar food resources between the two species. We found that the tree species composition of the breeding territories of the two species differed, mainly by a higher abundance of coniferous species around nest-boxes occupied by pied flycatchers. The temporal availability of caterpillars was measured using frass traps under four deciduous and two coniferous tree species. Deciduous tree species showed an early and narrow peak in abundance, which contrasted with the steady increase in caterpillar abundance in the coniferous tree species through the season. We subsequently calculated the predicted total caterpillar biomass available in each flycatcher territory. This differed between the species, with biomass decreasing more slowly in pied flycatcher territories. Caterpillar biomass is strongly correlated with the reproductive success of collared flycatchers, but much less so with pied flycatchers. However, caterpillar availability can only partly explain the differences in seasonal decline of reproductive success between the two species; we discuss additional factors that may contribute to this species difference. Overall, our results are consistent with the suggestion that minor habitat differences between these two species may contribute to promoting their coexistence.
    https://doi.org/10.1007/s00442-009-1544-1
  • Molecular Ecology
    2010

    Genome-wide SNP detection in the great tit Parus major using high throughput sequencing

    N.E.M. Van Bers, Kees van Oers, H.H.D. Kerstens, Bert W. Dibbits, R.P.M.A. Crooijmans, Marcel E. Visser, M.A.M. Groenen
    Identifying genes that underlie ecological traits will open exiting possibilities to study gene–environment interactions in shaping phenotypes and in measuring natural selection on genes. Evolutionary ecology has been pursuing these objectives for decades, but they come into reach now that next generation sequencing technologies have dramatically lowered the costs to obtain the genomic sequence information that is currently lacking for most ecologically important species. Here we describe how we generated over 2 billion basepairs of novel sequence information for an ecological model species, the great tit Parus major. We used over 16 million short sequence reads for the de novo assembly of a reference sequence consisting of 550 000 contigs, covering 2.5%of the genome of the great tit. This reference sequence was used as the scaffold for mapping of the sequence reads, which allowed for the detection of over 20 000 novel single nucleotide polymorphisms. Contigs harbouring 4272 of the single nucleotide polymorphisms could be mapped to a unique location on the recently sequenced zebra finch genome. Of all the great tit contigs, significantly more were mapped to the microchromosomes than to the intermediate and the macrochromosomes of the zebra finch, indicating a higher overall level of sequence conservation on the microchromosomes than on the other types of chromosomes. The large number of great tit contigs that can be aligned to the zebra finch genome shows that this genome provides a valuable framework for large scale genetics, e.g. QTL mapping or whole genome association studies, in passerines.
    https://doi.org/10.1111/j.1365-294X.2009.04486.x
  • Biology Letters
    2009

    Solar activity affects avian timing of reproduction

    Marcel E. Visser, J.J. Sanz
    Avian timing of reproduction is strongly affected by ambient temperature. Here we show that there is an additional effect of sunspots on laying date, from five long-term population studies of great and blue tits (Parus major and Cyanistes caeruleus), demonstrating for the first time that solar activity not only has an effect on population numbers but that it also affects the timing of animal behaviour. This effect is statistically independent of ambient temperature. In years with few sunspots, birds initiate laying late while they are often early in years with many sunspots. The sunspot effect may be owing to a crucial difference between the method of temperature measurements by meteorological stations (in the shade) and the temperatures experienced by the birds. A better understanding of the impact of all the thermal components of weather on the phenology of ecosystems is essential when predicting their responses to climate change.
    https://doi.org/10.1098/rsbl.2009.0429
  • Journal of Experimental Biology
    2009

    Temperature-induced elevation of basal metabolic rate does not affect testis growth in great tits

    Samuel P. Caro, Marcel E. Visser
    The timing of reproduction varies from year to year in many bird species. To adjust their timing to the prevailing conditions of that year, birds use cues from their environment. However, the relative importance of these cues, such as the initial predictive (e. g. photoperiod) and the supplemental factors (e. g. temperature), on the seasonal sexual development are difficult to distinguish. In particular, the fine-tuning effect of temperature on gonadal growth is not well known. One way temperature may affect timing is via its strong effect on energy expenditure as gonadal growth is an energy-demanding process. To study the interaction of photoperiod and temperature on gonadal development, we first exposed 35 individually housed male great tits (Parus major) to mid-long days (after 6 weeks of 8h L:16 h D at 15 degrees C, photoperiod was set to 13h L:11 h D at 15 degrees C). Two weeks later, for half of the males the temperature was set to 8 degrees C, and for the other half t! o 22 degrees C. Unilateral laparotomies were performed at weeks 5 (i.e one week before the birds were transferred to mid-long days), 8 and 11 to measure testis size. Two measures of basal metabolic rate (BMR) were performed at the end of the experiment (weeks 11 and 12). Testis size increased significantly during the course of the experiment, but independently of the temperature treatment. BMR was significantly higher in birds exposed to the cold treatment. These results show that temperature-related elevation of BMR did not impair the long-day-induced testis growth in great tits. As a consequence, temperature may not be a crucial cue and/or constraint factor in the fine-tuning of the gonadal recrudescence in male great tits, and testis growth is not a high energy-demanding seasonal process.
    https://doi.org/10.1242/jeb.026344
  • Global Change Biology
    2009

    Climate change leads to decreasing bird migration distances

    Marcel E. Visser, A.C. Perdeck, J.H. Van Balen, Christiaan Both
    Global climate change has led to warmer winters in NW Europe, shortening the distance between suitable overwintering areas and the breeding areas of many bird species. Here we show that winter recovery distances have decreased over the past seven decades, for birds ringed during the breeding season in the Netherlands between 1932 and 2004. Of the 24 species included in the analysis, we found in 12 a significant decrease of the distance to the wintering site. Species from dry, open areas shortened their distance the most, species from wet, open areas the least, while woodland species fall in between the other two habitats. The decline in migration distance is likely due to climate change, as migration distances are negatively correlated with the Dutch temperatures in the winter of recovery. With a shorter migration distance, species should be better able to predict the onset of spring at their breeding sites and this could explain the stronger advancement of arrival date found in several short distance species relative to long-distance migrants.
    https://doi.org/10.1111/j.1365-2486.2009.01865.x
  • Journal of Animal Ecology
    2009

    Climate change and unequal phenological changes across four trophic levels: constraints or adaptations?

    Christiaan Both, M. Van Asch, R.G. Bijlsma, A.B. Van den Burg, Marcel E. Visser
    1. Climate change has been shown to affect the phenology of many organisms, but interestingly these shifts are often unequal across trophic levels, causing a mismatch between the phenology of organisms and their food. 2. We consider two alternative hypotheses: consumers are constrained to adjust sufficiently to the lower trophic level, or prey species react more strongly than their predators to reduce predation. We discuss both hypotheses with our analyses of changes in phenology across four trophic levels: tree budburst, peak biomass of herbivorous caterpillars, breeding phenology of four insectivorous bird species and an avian predator. 3. In our long-term study, we show that between 1988 and 2005, budburst advanced (not significantly) with 0·17 d yr−1, while between 1985 and 2005 both caterpillars (0·75 d year−1) and the hatching date of the passerine species (range for four species: 0·36–0·50 d year−1) have advanced, whereas raptor hatching dates showed no trend. 4. The caterpillar peak date was closely correlated with budburst date, as were the passerine hatching dates with the peak caterpillar biomass date. In all these cases, however, the slopes were significantly less than unity, showing that the response of the consumers is weaker than that of their food. This was also true for the avian predator, for which hatching dates were not correlated with the peak availability of fledgling passerines. As a result, the match between food demand and availabili 5. These results could equally well be explained by consumers' insufficient responses as a consequence of constraints in adapting to climate change, or by them trying to escape predation from a higher trophic level, or both. Selection on phenology could thus be both from matches of phenology with higher and lower levels, and quantifying these can shed new light on why some organisms do adjust their phenology to climate change, while others do not.
    https://doi.org/10.1111/j.1365-2656.2008.01458.x
  • Proceedings of the Royal Society B-Biological Sciences
    2009

    Temperature has a causal effect on avian timing of reproduction

    Marcel E. Visser, L.J.M. Holleman, Samuel P. Caro
    Many bird species reproduce earlier in years with high spring temperatures, but little is known about the causal effect of temperature. Temperature may have a direct effect on timing of reproduction but the correlation may also be indirect, for instance via food phenology. As climate change has led to substantial shifts in timing, it is essential to understand this causal relationship to predict future impacts of climate change. We tested the direct effect of temperature on laying dates in great tits (Parus major) using climatized aviaries in a 6-year experiment. We mimicked the temperature patterns from two specific years in which our wild population laid either early (‘warm’ treatment) or late (‘cold’ treatment). Laying dates were affected by temperature directly. As the relevant temperature period started three weeks prior to the mean laying date, with a range of just 4°C between the warm and the cold treatments, and as the birds were fed ad libitum, it is likely that temperature acted as a cue rather than lifting an energetic constraint on the onset of egg production. We furthermore show a high correlation between the laying dates of individuals reproducing both in aviaries and in the wild, validating investigations of reproduction of wild birds in captivity. Our results demonstrate that temperature has a direct effect on timing of breeding, an important step towards assessing the implication of climate change on seasonal timing.
    https://doi.org/10.1098/rspb.2009.0213
  • Proceedings of the Royal Society B-Biological Sciences
    2004

    Central assumptions of predator-prey models fail in a semi-natural experimental system

    C.M.M. Mols, Kees van Oers, L.M.A. Witjes, Kate Lessells, P.J. Drent, Marcel E. Visser
    The relationship between the encounter rate of predators with prey and the density of this prey is fundamental to models of predator-prey interactions. The relationship determines, among other variables, the rate at which prey patches are depleted, and hence the impact of predator populations on their prey, and the optimal spatial distribution of foraging effort. Two central assumptions that are made in many models are that encounter rate is directly proportional to prey density and that it is independent of the proportion of prey already removed, other than via the decreased density. We show here, using captive great tits searching for winter moth caterpillars in their natural hiding positions, that neither of these assumptions hold. Encounter rate increased less than directly in proportion to prey density, and it depended not only on the current density of prey, but also on the proportion of prey already removed by previous foragers. Both of these effects are likely to have major consequences for the outcome of predator-prey interactions.
    https://doi.org/10.1098/rsbl.2003.0110

Projecten & samenwerkingen

Projecten

Outreach

See for my contribution to the UN Environmental Program contribution in Frontiers 2022: Noise, Blazes and Mismatches here

See my presentation for the BioClock Academy on Seasonal Timing here

Categorieën