Kees van Oers

Prof. dr. Kees van Oers

Senior Researcher
Send message

Visiting Address

Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands

About

The world is constantly changing partly due to human influences. My goal is to find answers to questions related to individual responses to changing environments. I do this from an evolutionary point of view, at the crossroads between ecology and genomics.

Biography

The world around us is changing and individuals of many species need to cope with these changes in order to thrive. The notion that individuals within species consistently vary in coping with such challenges, comparable to how humans differ in their personality and cognition, has only recently been recognised. The van Oers group was at the cradle of the research field of animal personality that has now rooted in all biological disciplines. By combining detailed experimental work on captive animals with studies in natural populations, the work of the group is generally recognised as the most comprehensive evolutionary study on animal personality. Since behaviour is affected by both heritable and environmental aspects, our findings show that in all aspects of an organism ranging from the genetic make-up to fitness, individual consistency needs to be taken into account in order to be able to predict how individuals, species and eventually ecosystems will respond to global environmental change, such a climate change and urbanisation.

Our work is recognised by the general public, since it is close to their experiences that animals, such as pets have personalities on their own. The work on animal personality directly affected the way of thinking about animals and has opened up discussions about animal welfare, species conservation and human-animal relationships. As specific case the great is used, which for example is a pest species to fruit growers, but seen as saviours in the fight against Oak procession caterpillar nuisance. In this way the extensive long-term work on our study system is translated to applicable knowledge.

Research groups

CV

Employment

  • 2012–Present
    Senior Scientist, Dept. Animal Ecology, NIOO-KNAW
  • 2018–Present
    Professor in Animal Personality at the Behavioural Ecology Group (Wageningen University & Research)
  • 2009–2012
    Research Scientist, Dpt. Animal Ecology (NIOO-KNAW)
  • 2006–2009
    VENI Research Associate, Dpt. Animal Ecology (NIOO-KNAW)
  • 2004–2006
    Postdoctoral fellow, Max-Planck Institute for Ornithology, Seewiesen, Germany
  • 1998–2004
    PhD student, Dpt. Animal Ecology (NIOO-KNAW)

Education

  • 1990–1994
    BSc Ecology, Utrecht University
  • 1994–1996
    MSc Animal Ecology, Groningen University

Editorial board memberships

  • 2018–Present
    Behavioral Ecology and Sociobiology
  • 2013–2016
    Animal Behaviour
  • 2010–2012
    ARDEA

PhD students

  • 2018–Present
    Krista van den Heuvel
    NIOO-KNAW, WUR
    Promotors: Kees van Oers, co-promotor Alexander Kotrschal (WUR)
  • 2018–Present
    Bernice Sepers
    NIOO-KNAW, WUR
    Promotors: Kees van Oers, co-promotor Koen Verhoeven
  • 2016–2020
    Nina Bircher
    WUR, NIOO-KNAW
    Promotors: Marc Naguib (WUR) and Kees van Oers
  • 2014–2018
    Lies Zandberg
    WUR, NIOO-KNAW
    Promotors: Marc Naguib (WUR), co-promotor Camilla Hinde (WUR) and Kees van Oers
  • 2010–2015
    Lysanne Snijders
    WUR, NIOO-KNAW
    Promotors: Marc Naguib (WUR), co-promotor Kees van Oers
  • 2005–2009
    Eva Fucikova
    NIOO-KNAW, University Groningen
    Promotors: Marcel Visser, co-promotor Kees van Oers and Piet Drent
  • 2021–Present
    Rebecca Shuhua Chen
    University of Bielefeld, University of Lincoln, Netherlands Institute of Ecology (NIOO-KNAW)
    Promotors: Joe Hoffman, Carl Soulsbury, Kees van Oers

Ancillary activities

Publications

Peer-reviewed publications

  • 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 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
  • Molecular Ecology Resources
    2022

    epiGBS2

    F. Gawehns, Maarten Postuma, Morgane Van Antro, Adam Nunn, Bernice Sepers, Samar Fatma, Thomas Van Gurp, Niels C. A. M. Wagemaker, A.C. Mateman, Slavica Milanovic-Ivanovic, Ivo Groβe, Kees van Oers, Philippine Vergeer, Koen Verhoeven

    Several reduced-representation bisulfite sequencing methods have been developed in recent years to determine cytosine methylation de novo in nonmodel species. Here, we present epiGBS2, a laboratory protocol based on epiGBS with a revised and user-friendly bioinformatics pipeline for a wide range of species with or without a reference genome. epiGBS2 is cost- and time-efficient and the computational workflow is designed in a user-friendly and reproducible manner. The library protocol allows a flexible choice of restriction enzymes and a double digest. The bioinformatics pipeline was integrated in the Snakemake workflow management system, which makes the pipeline easy to execute and modular, and parameter settings for important computational steps flexible. We implemented bismark for alignment and methylation analysis and we preprocessed alignment files by double masking to enable single nucleotide polymorphism calling with Freebayes (epiFreebayes). The performance of several critical steps in epiGBS2 was evaluated against baseline data sets from Arabidopsis thaliana and great tit (Parus major), which confirmed its overall good performance. We provide a detailed description of the laboratory protocol and an extensive manual of the bioinformatics pipeline, which is publicly accessible on github (https://github.com/nioo-knaw/epiGBS2) and zenodo (https://doi.org/10.5281/zenodo.4764652).

    https://doi.org/10.1111/1755-0998.13597
  • Behavioral Ecology and Sociobiology
    2022

    No reproductive fitness benefits of dear enemy behaviour in a territorial songbird

    Michael S. Reichert, Jodie M.S. Crane, Gabrielle L. Davidson, Eileen Dillane, Ipek G. Kulahci, James O’Neill, Kees van Oers, Ciara Sexton, John L. Quinn

    Territorial animals often respond less aggressively to neighbours than strangers. This ‘dear enemy’ effect is hypothesized to be adaptive by reducing unnecessary aggressive interactions with non-threatening individuals. A key prediction of this hypothesis, that individual fitness will be affected by variation in the speed and the extent to which individuals reduce their aggression towards neighbours relative to strangers, has never been tested. We used a series of song playbacks to measure the change in response of male great tits to a simulated establishment of a neighbour on an adjacent territory during early stages of breeding, as an assay of individuals’ tendencies to form dear enemy relationships. Males reduced their approach to the speaker and sang fewer songs on later playback repetitions. However, only some males exhibited dear enemy behaviour by responding more strongly to a subsequent stranger playback, and when the playback procedure was repeated on a subset of males, there was some indication for consistent differences among individuals in the expression of dear enemy behaviour. We monitored nests and analysed offspring paternity to determine male reproductive success. Individuals that exhibited dear enemy behaviour towards the simulated neighbour did not suffer any costs associated with loss of paternity, but there was also no evidence of reproductive benefits, and no net effect on reproductive fitness. The general ability to discriminate between neighbours and strangers is likely adaptive, but benefits are probably difficult to detect because of the indirect link between individual variation in dear enemy behaviour and reproductive fitness and because of the complex range of mechanisms affecting relations with territorial neighbours. Significance statement: The dear enemy effect, in which animals respond less aggressively to familiar neighbours compared to strangers, is probably beneficial because it reduces aggressive interactions with non-threatening individuals. However, no study has ever tested whether there actually are fitness benefits for individuals with a greater tendency to form dear enemy relationships. Our study used experimental playbacks to simulate neighbours and strangers, and we found no relationship between dear enemy behaviour and reproductive success in a songbird. However, our approach to test adaptive hypotheses of this widespread territorial behaviour and our longitudinal playback design to examine the development of familiarity towards a neighbour and discrimination of neighbours and strangers are likely to be important tools to advance our understanding of territorial behaviour and individual recognition.

    https://doi.org/10.1007/s00265-022-03199-1
  • Behavioral Ecology and Sociobiology
    2022

    Prior territorial responses and home range size predict territory defense in radio-tagged great tits

    Marc Naguib, Mieke Titulaer, J.R. Waas, Kees van Oers, Philipp Sprau, Lysanne Snijders

    Territorial animals often use signals to advertise territorial occupancy within their larger home ranges. Songbirds are among the best-studied territorial signaling taxa, and when competitors start singing during a territorial intrusion, residents usually show elevated spatial and vocal responses. These responses could be used by intruders and distant eavesdroppers to predict future responses or to compare responses across competitors. Yet, the extent to which responses of a resident to a territorial intrusion predict its future responses and its overall spatial behavior (home range) within a neighborhood is less well understood. We used wild great tits (Parus major) as a model species in repeated song playback trials, simulating territorial intrusions combined with radio-tracking before and during playback trials. The time spent close to the loudspeaker in response to an initial simulated intrusion predicted the same response variable during a second simulated intrusion on the next day, whereas singing activity during the first simulated intrusion did not predict singing during the second simulated intrusion. We also show that more explorative males (as determined by a novel environment test) and males with smaller home ranges sang more and spent more time near the loudspeaker in response to both simulated intrusions. Thus, by probing residents, intruders can obtain reliable information about subsequent response probabilities, while eavesdroppers from a distance, who can use auditory information only, would not receive sufficient predictive information. Our findings also suggest that males with larger home ranges are more tolerant toward intruders, which could reflect a trade-off between tendencies to respond strongly and to range widely. The lack of predictability of singing activity with regard to responses to future intrusions might explain why territorial animals continuously exchange vocal signals and regularly foray into neighboring territories, as a way to obtain regular information updates. Significance Statement: Animals use experience from interactions with conspecifics in their future decision making, such as mate choice and strategies for conflict resolution. The value of such information depends in part on the predictability of the future behavior of that conspecific. In songbirds, territorial individuals respond to intruders by approach and signaling. Here, we tested in radio-tagged great tits (Parus major) if territorial responses are predictable and are affected by individual and environmental factors. We show that the time spent near the simulated intruder was more predictable than singing activity and that birds with larger home ranges showed weaker responses. These findings suggest that information based on such spatial responses is more useful for future decision making, as compared to vocal information, and that distant eavesdroppers will thus receive less reliable information. Limited predictability may explain why territorial animals continuously exchange vocal signals and foray into neighboring territories, providing opportunities for regular information updates.

    https://doi.org/10.1007/s00265-022-03143-3
  • Molecular Ecology Resources
    2022

    An ecologist's guide for studying DNA methylation variation in wild vertebrates

    Veronika Laine, Bernice Sepers, Melanie Lindner, F. Gawehns, Suvi Ruuskanen, Kees van Oers

    The field of molecular biology is advancing fast with new powerful technologies, sequencing methods and analysis software being developed constantly. Commonly used tools originally developed for research on humans and model species are now regularly used in ecological and evolutionary research. There is also a growing interest in the causes and consequences of epigenetic variation in natural populations. Studying ecological epigenetics is currently challenging, especially for vertebrate systems, because of the required technical expertise, complications with analyses and interpretation, and limitations in acquiring sufficiently high sample sizes. Importantly, neglecting the limitations of the experimental setup, technology and analyses may affect the reliability and reproducibility, and the extent to which unbiased conclusions can be drawn from these studies. Here, we provide a practical guide for researchers aiming to study DNA methylation variation in wild vertebrates. We review the technical aspects of epigenetic research, concentrating on DNA methylation using bisulfite sequencing, discuss the limitations and possible pitfalls, and how to overcome them through rigid and reproducible data analysis. This review provides a solid foundation for the proper design of epigenetic studies, a clear roadmap on the best practices for correct data analysis and a realistic view on the limitations for studying ecological epigenetics in vertebrates. This review will help researchers studying the ecological and evolutionary implications of epigenetic variation in wild populations.

    https://doi.org/10.1111/1755-0998.13624
  • 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
  • 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
  • Environmental Science and Technology
    06-07-2021

    Does Arsenic Contamination Affect DNA Methylation Patterns in a Wild Bird Population? An Experimental Approach

    Veronika Laine, Mark Verschuuren, Kees van Oers, Silvia Espín, Pablo Sánchez-Virosta, Tapio Eeva, Suvi Ruuskanen

    Pollutants, such as toxic metals, negatively influence organismal health and performance, even leading to population collapses. Studies in model organisms have shown that epigenetic marks, such as DNA methylation, can be modulated by various environmental factors, including pollutants, influencing gene expression, and various organismal traits. Yet experimental data on the effects of pollution on DNA methylation from wild animal populations are largely lacking. We here experimentally investigated for the first time the effects of early-life exposure to environmentally relevant levels of a key pollutant, arsenic (As), on genome-wide DNA methylation in a wild bird population. We experimentally exposed nestlings of great tits (Parus major) to arsenic during their postnatal developmental period (3 to 14 days post-hatching) and compared their erythrocyte DNA methylation levels to those of respective controls. In contrast to predictions, we found no overall hypomethylation in the arsenic group. We found evidence for loci to be differentially methylated between the treatment groups, but for five CpG sites only. Three of the sites were located in gene bodies of zinc finger and BTB domain containing 47 (ZBTB47), HIVEP zinc finger 3 (HIVEP3), and insulin-like growth factor 2 mRNA binding protein 1 (IGF2BP1). Further studies are needed to evaluate whether epigenetic dysregulation is a commonly observed phenomenon in polluted populations and what are the consequences for organism functioning and for population dynamics.

    https://doi.org/10.1021/acs.est.0c08621
  • Animal Behaviour
    06-2021

    Anyone listening? No evidence for eavesdropping on male singing interactions in the great tit, Parus major

    Nina Bircher, Kees van Oers, Marc Naguib

    Observing interactions between others can provide important information to individuals. Male songbirds often engage in singing contests where they vary the type and timing of signals and provide eavesdropping individuals with information about their competitiveness. How this information is used and its effect on subsequent spatial behaviour and reproductive decisions of eavesdroppers is not well understood. Here we tested whether great tits use information gathered by eavesdropping on male singing interactions to assess rivals and (potential) mates. We used interactive playback experiments to engage territorial males in song contests with either a more (song overlapping and more persistent singing) or less challenging (song alternating and less persistent singing) intruder. We followed male and female movements by automated radiotracking, determined paternity using microsatellite analysis and maternal investment by quantifying egg weights and provisioning behaviour. We expected that mates of males exposed to the challenging treatment would subsequently foray more often off territory to assess other males and potential extrapair mates and invest less in their broods. Moreover, we expected that neighbours would adjust their foraying behaviour according to information gained by eavesdropping. Females, however, did not alter their foraying behaviour or brood investment and neither female nor male neighbours changed their visiting behaviour to playback territories. Our results provide no evidence that females used information gathered by eavesdropping on asymmetric song interactions in reproductive decisions or that song interactions affected movements across territories in the neighbourhood. Overlapping or singing for a longer time on an intruded upon territory may not always be perceived as a higher level of threat, and reproductive decisions and assessment of familiar individuals are likely to be based on multiple sources of information rather than on a single interaction.

    https://doi.org/10.1016/j.anbehav.2021.03.009
  • Animal Behaviour
    04-2021

    Motivation, accuracy and positive feedback through experience explain innovative problem solving and its repeatability

    Amy C. Cooke, Gabrielle L. Davidson, Kees van Oers, John L. Quinn
    Adapting to environmental change is a major challenge faced by animals and the role of individual behavioural differences in facilitating this process is currently the focus of much research. Innovation, the generation of a novel behaviour or use of a known behaviour in a novel context, is one form of behaviour that enables animals to respond to change. By deciphering the mechanisms underlying innovativeness, especially those that explain consistent differences between individuals, we can further understand the consequences of this behavioural variation. We tested whether motivation, experience, inhibitory control and personality were linked to different stages of sequential innovative problem-solving performance among great tits, Parus major, and of their overall innovativeness across tasks. We gave animals originating from lines bidirectionally selected for fast or slow early exploratory behaviour, a multiaccess problem-solving device. Diverse motor skills and behavioural flexibility were required to solve all three different access points sequentially over trials. Food-deprived, highly motivated birds had shorter latency to touch the device, were more likely to solve an access point within a trial, and solved a greater diversity of them, than their less motivated counterparts. Solving success increased with accuracy when interacting with the device (proportion of touches to functional components of the device compared to all touches to the device per trial), and with previous experience. Personality selection lines and inhibitory control had little effect. Repeatability analysis showed that between-individual differences in problem-solving performance were explained by: (1) pseudorepeatable effects (upward bias) linked to hunger-induced motivation, (2) repeatable differences in accuracy when interacting with devices, and (3) a feedback loop caused by experience gained over successive trials. Our results highlight the challenges of characterizing consistent individual differences in behaviour generally and support the idea that complex sources of variation play an important role in problem-solving performance.
    https://doi.org/10.1016/j.anbehav.2021.01.024
  • Frontiers in Ecology and Evolution
    04-03-2021

    Epigenetics and Early Life Stress: Experimental Brood Size Affects DNA Methylation in Great Tits (Parus major)

    Bernice Sepers, Jolijn Erven, F. Gawehns, Veronika Laine, Kees van Oers
    Early developmental conditions are known to have life-long effects on an individual’s behavior, physiology and fitness. In altricial birds, a majority of these conditions, such as the number of siblings and the amount of food provisioned, are controlled by the parents. This opens up the potential for parents to adjust the behavior and physiology of their offspring according to local post-natal circumstances. However, the mechanisms underlying such intergenerational regulation remain largely unknown. A mechanism often proposed to possibly explain how parental effects mediate consistent phenotypic change is DNA methylation. To investigate whether early life effects on offspring phenotypes are mediated by DNA methylation, we cross-fostered great tit (Parus major) nestlings and manipulated their brood size in a natural study population. We assessed genome-wide DNA methylation levels of CpG sites in erythrocyte DNA, using Reduced Representation Bisulfite Sequencing (RRBS). By comparing DNA methylation levels between biological siblings raised in enlarged and reduced broods and between biological siblings of control broods, we assessed which CpG sites were differentially methylated due to brood size. We found 32 differentially methylated sites (DMS) between siblings from enlarged and reduced broods, a larger number than in the comparison between siblings from control broods. A considerable number of these DMS were located in or near genes involved in development, growth, metabolism, behavior and cognition. Since the biological functions of these genes line up with previously found effects of brood size and food availability, it is likely that the nestlings in the enlarged broods suffered from nutritional stress. We therefore conclude that early life stress might directly affect epigenetic regulation of genes related to early life conditions. Future studies should link such experimentally induced DNA methylation changes to expression of phenotypic traits and assess whether these effects affect parental fitness to determine if such changes are also adaptive.
    https://doi.org/10.3389/fevo.2021.609061
  • Epigenetics
    2021

    The effect of experimental lead pollution on DNA methylation in a wild bird population

    Hannu Mäkinen, Kees van Oers, Tapio Eeva, Suvi Ruuskanen

    Anthropogenic pollution is known to negatively influence an organism’s physiology, behaviour, and fitness. Epigenetic regulation, such as DNA methylation, has been hypothesized as a potential mechanism to mediate such effects, yet studies in wild species are lacking. We first investigated the effects of early-life exposure to the heavy metal lead (Pb) on DNA methylation levels in a wild population of great tits (Parus major), by experimentally exposing nestlings to Pb at environmentally relevant levels. Secondly, we compared nestling DNA methylation from a population exposed to long-term heavy metal pollution (close to a copper smelter), where birds suffer from pollution-related decrease in food quality, and a control population. For both comparisons, the analysis of about one million CpGs covering most of the annotated genes revealed that pollution-related changes in DNA methylation were not genome wide, but enriched for genes underlying developmental processes. However, the results were not consistent when using binomial or beta binomial regression highlighting the difficulty of modelling variance in CpGs. Our study indicates that post-natal anthropogenic heavy metal exposure can affect methylation levels of development related genes in a wild bird population.

    https://doi.org/10.1080/15592294.2021.1943863
  • Proceedings of the National Academy of Sciences of the United States of America
    2021

    Heterogeneous selection on exploration behavior within and among West European populations of a passerine bird

    Alexia Mouchet, Ella F. Cole, Erik Matthysen, Marion Nicolaus, John L. Quinn, Allison M. Roth, J.M. Tinbergen, Kees van Oers, Thijs van Overveld, N.J. Dingemanse

    Heterogeneous selection is often proposed as a key mechanism maintaining repeatable behavioral variation ("animal personality") in wild populations. Previous studies largely focused on temporal variation in selection within single populations. The relative importance of spatial versus temporal variation remains unexplored, despite these processes having distinct effects on local adaptation. Using data from >3,500 great tits (Parus major) and 35 nest box plots situated within five West-European populations monitored over 4 to 18 y, we show that selection on exploration behavior varies primarily spatially, across populations, and study plots within populations. Exploration was, simultaneously, selectively neutral in the average population and year. These findings imply that spatial variation in selectionmay represent a primarymechanism maintaining animal personalities, likely promoting the evolution of local adaptation, phenotype-dependent dispersal, and nonrandom settlement. Selection also varied within populations among years, which may counteract local adaptation. Our study underlines the importance of combining multiple spatiotemporal scales in the study of behavioral adaptation.

    https://doi.org/10.1073/pnas.2024994118
  • 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, S.J.G. Vriend, Zuzana Zajkova, Peter Adamík, Lucy M. Aplin, Elena Angulo, Alexandr 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 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 Cláudia 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
  • 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 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
  • Current Biology
    10-08-2020

    How the COVID-19 pandemic highlights the necessity of animal research

    Lisa Genzel, Roger A H Adan, Anton Berns, Jeroen van den Beucken, Arjan Blokland, Erik H.W.G.M. Boddeke, Willy M. Bogers, Ronald Bontrop, R. Bulthuis, Teun Bousema, Hans Clevers, Tineke C.J.J. Coenen, Anne-Marie van Dam, Peter M.T. Deen, Ko Willems van Dijk, Bart J L Eggen, Ype Elgersma, Izel Erdogan, Bernard Englitz, J. Martje Fentener van Vlissingen, Susanne E la Fleur, Ron A. M. Fouchier, P. Fitzsimons Carlos, Wilbert Frieling, Bart Haagmans, Balthasar A. Heesters, Marloes Henckens, Sander Herfst, Elly Hol, Daniel van den Hove, Marien I. de Jonge, Jos Jonkers, Leo A B Joosten, A. Kalsbeek, M. Kamermans, Harm H. Kampinga, Martien J H Kas, Jaap Keijer, Sander Kersten, Amanda J. Kiliaan, Taco W.A. Kooij, Sander Kooijman, W. Koopman, Aniko Korosi, Harm J Krugers, Thijs Kuiken, Steven A Kushner, Jan A.M. Langermans, Heidi Lesscher, Paul J Lucassen, Esther Lutgens, Mihai G Netea, Lucas P.J.J. Noldus, Jos W M van der Meer, Frank J Meye, Joram David Mul, Kees van Oers, Jocelien D. A. Olivier, R Jeroen Pasterkamp, Ingrid H.C.H.M. Philippens, Jos Prickaerts, Bart Pullox, Patrick C N Rensen, Jacco van Rheenen, Ronald P. van Rij, Laila Ritsma, Barry.H.G. Rockx, Benno Roozendaal, Evert M. van Schothorst, K. Stittelaar, Norbert Stockhofe, D.F. Swaab, Rik L. de Swart, Louk J M J Vanderschuren, Taco de Vries, Femke M S de Vrij, Richard van Wezel, Corette J Wierenga, Maximilian Wiesmann, Ingo Willuhn, C.I. De Zeeuw, Judith Homberg
    Recently, a petition was offered to the European Commission calling for an immediate ban on animal testing. Although a Europe-wide moratorium on the use of animals in science is not yet possible, there has been a push by the non-scientific community and politicians for a rapid transition to animal-free innovations. Although there are benefits for both animal welfare and researchers, advances on alternate methods have not progressed enough to be able to replace animal research in the foreseeable future. This trend has led first and foremost to a substantial increase in the administrative burden and hurdles required to make timely advances in research and treatments for human and animal diseases. The current COVID-19 pandemic clearly highlights how much we actually rely on animal research. COVID-19 affects several organs and systems, and various animal-free alternatives currently available do not even come close to this complexity. In this Essay we therefore argue that the use of animals is essential for the advancement of human and veterinary health.
    https://doi.org/10.1016/j.cub.2020.08.030
  • Behavioral Ecology
    2020

    Extraterritorial forays by great tits are associated with dawn song in unexpected ways

    Nina Bircher, Kees van Oers, C.A. Hinde, Marc Naguib
    Conspicuous male signals often play an important role in both attracting mates and deterring rivals. In territorial species with extrapair mating, female and male forays to other territories may be an important component underlying female choice and male mating success and might be influenced by male advertisement signals. Yet, whether off-territory foraying is associated with male signals is still not well understood. Here, we tested how female and male forays are associated with short-range visual and long-range acoustic signals (dawn song). We used an automated radio tracking system to follow the movements of wild great tits (Parus major) to other territories in relation to male dawn song, plumage ornaments, and extrapair paternity. We show that both sexes frequently forayed into others’ territories throughout the breeding period. Movements of both males and females were associated with male song but not with plumage ornaments. Contrary to our expectations, females stayed away from territories where males sang elaborately, whereas males were attracted to those territories. Moreover, neither female nor male forays were associated with the occurrence of extrapair offspring. Our results, thus, suggest that, although forays into other territories are associated with male dawn song, females may not be attracted and males not repelled by dawn song. This sheds a different light on the sex-specific effects of male advertisement signals, expanding the view on the selection pressures shaping such communication systems.
    https://doi.org/10.1093/beheco/araa040
  • Integrative and Comparative Biology
    2020

    Epigenetics of animal personality

    Kees van Oers, Bernice Sepers, W. Sies, F. Gawehns, Koen Verhoeven, Veronika Laine
    The search for the hereditary mechanisms underlying quantitative traits traditionally focused on the identification of underlying genomic polymorphisms such as single-nucleotide polymorphisms. It has now become clear that epigenetic mechanisms, such as DNA methylation, can consistently alter gene expression over multiple generations. It is unclear, however, if and how DNA methylation can stably be transferred from one generation to the next and can thereby be a component of the heritable variation of a trait. In this study, we explore whether DNA methylation responds to phenotypic selection using whole-genome and genome-wide bisulfite approaches. We assessed differential erythrocyte DNA methylation patterns between extreme personality types in the Great Tit (Parus major). For this, we used individuals from a four-generation artificial bi-directional selection experiment and siblings from eight F2 inter-cross families. We find no differentially methylated sites when comparing the selected personality lines, providing no evidence for the so-called epialleles associated with exploratory behavior. Using a pair-wise sibling design in the F2 intercrosses, we show that the genome-wide DNA methylation profiles of individuals are mainly explained by family structure, indicating that the majority of variation in DNA methylation in CpG sites between individuals can be explained by genetic differences. Although we found some candidates explaining behavioral differences between F2 siblings, we could not confirm this with a whole-genome approach, thereby confirming the absence of epialleles in these F2 intercrosses. We conclude that while epigenetic variation may underlie phenotypic variation in behavioral traits, we were not able to find evidence that DNA methylation can explain heritable variation in personality traits in Great Tits.
    https://doi.org/10.1093/icb/icaa138
  • Proceedings of the Royal Society B-Biological Sciences
    2020

    Anthropogenic noise impairs foraging for cryptic prey via cross-sensory interference

    Wouter Halfwerk, Kees van Oers
    Anthropogenic noise levels are globally rising with profound impacts on ecosystems and the species that live in them. Masking or distraction by noise can interfere with relevant sounds and thereby impact ecological interactions between individuals of the same or different species. Predator–prey dynamics are particularly likely to be influenced by rising noise levels, with important population- and community-level consequences, as species may differentially adapt to noise disturbance. Acoustic noise can, however, also impair the use of visual information by animals through the process of cross-sensory interference, possibly impacting species interactions that have so far been largely ignored by noise impact studies. Here, we assessed how noise affected the performance of great tit (Parus major) foraging on cryptic prey. Birds trained individually to search for paper moths differing in the level of camouflage with the test background were tested in the presence and absence of noise. We found that noise significantly increased approach and attack latencies, but that the effect depended on the level of crypsis. Noise increased latencies for cryptic prey targets, but not for conspicuous and colour-matched prey targets. Our results show that noise can interfere with the processing of visual information, particularly in difficult tasks such as separating objects from a similar looking background. These results have important ecological and evolutionary implications as they demonstrate how globally rising anthropogenic noise levels can influence the arms race between predators and prey across sensory domains.
    https://doi.org/10.1098/rspb.2019.2951
  • Animal Behaviour
    2020

    Measuring mate preferences: Absolute and comparative evaluation of potential partners

    Lies Zandberg, C.A. Hinde, Kees van Oers
    Quantifying the direction and strength of mate preference is essential to improve our understanding of sexual selection. Experimental designs, however, often do not consider how individuals evaluate and compare the available options, which may affect the results significantly. Preferences are often assumed to be absolute, with individuals assigning a fixed, absolute value to a cue or potential partner they encounter. However, individuals may instead also compare the available options, in which case the social context plays an essential role in the preference for each potential partner. Here we investigated the importance of considering the choosers’ evaluation process in mate preference tests. Using a mate preference study on wild great tit, Parus major, heterozygosity, breast stripe size and yellowness as a case study, we tested whether individuals use absolute or comparative mate preferences. We analysed how the perceived average attractiveness and the variation in attractiveness of the group of potential mates affected the measured preference functions. We found that the average attractiveness of the stimulus groups affected the total time individuals spent visiting all stimulus birds, and that the variation in attractiveness within groups affected the measured preference slopes. This indicates that the social context will affect the measured responses to stimulus groups, and that great tits may use both absolute and comparative evaluation. Considering how a study species encounters and evaluates potential mates and how the social environment may affect preferences is essential when choosing an appropriate experimental design to obtain reliable measurements of mate preferences. We therefore strongly advise future studies to consider not only the absolute stimulus trait values, but also the context in which they are presented. The ability to quantify preferences accurately will increase our understanding of mate preferences, mate choice and ultimately sexual selection.
    https://doi.org/10.1016/j.anbehav.2020.06.019
  • 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
  • Ecology and Evolution
    01-08-2019

    Exploratory behavior undergoes genotype–age interactions in a wild bird

    Barbara Class, Jon E Brommer, Kees van Oers
    Abstract Animal personality traits are often heritable and plastic at the same time. Indeed, behaviors that reflect an individual's personality can respond to environmental factors or change with age. To date, little is known regarding personality changes during a wild animals' lifetime and even less about stability in heritability of behavior across ages. In this study, we investigated age-related changes in the mean and in the additive genetic variance of exploratory behavior, a commonly used measure of animal personality, in a wild population of great tits. Heritability of exploration is reduced in adults compared to juveniles, with a low genetic correlation across these age classes. A random regression animal model confirmed the occurrence of genotype?age interactions (G?A) in exploration, causing a decrease in additive genetic variance before individuals become 1 year old, and a decline in cross-age genetic correlations between young and increasingly old individuals. Of the few studies investigating G?A in behaviors, this study provides rare evidence for this phenomenon in an extensively studied behavior. We indeed demonstrate that heritability and cross-age genetic correlations in this behavior are not stable over an individual's lifetime, which can affect its potential response to selection. Because G?A is likely to be common in behaviors and have consequences for our understanding of the evolution of animal personality, more attention should be turned to this phenomenon in the future work.
    https://doi.org/10.1002/ece3.5430
  • Journal of Ornithology
    10-07-2019

    Avian ecological epigenetics: pitfalls and promises

    Bernice Sepers, Krista van den Heuvel, Melanie Lindner, Heidi Viitaniemi, Arild Husby, Kees van Oers
    Epigenetic mechanisms can alter gene expression without a change in the nucleotide sequence and are increasingly recognized as important mechanisms that can generate phenotypic diversity. Most of our current knowledge regarding the origin and role of epigenetic variation comes from research on plants or mammals, often in controlled rearing conditions. Epigenetic research on birds in their natural habitats is still in its infancy, but is needed to answer questions regarding the origin of epigenetic marks and their role in phenotypic variation and evolution. Here we review the potential for studying epigenetic variation in natural bird systems. We aim to provide insights into (1) the origin of epigenetic variation, (2) the relationship between epigenetic variation and trait variation, and (3) the possible role of epigenetic variation in adaptation to changing environments. As there is currently little research on epigenetics in wild birds, we examine how findings on other taxa such as plants and mammals relate to birds. We also examine some of the pros and cons of the most commonly used methods to study patterns of DNA methylation in birds, and suggest some topics we believe need to be addressed to develop the field of wild avian epigenetics further.
    https://doi.org/10.1007/s10336-019-01684-5
  • 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 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
  • 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 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
  • Animal Behaviour
    2019

    Personality types vary in their personal and social information use

    Judith Smit, Kees van Oers
    Gathering information about the environment, such as the location and quality of food, is crucial for an animal's survival, particularly in a changing environment. An animal can collect ‘personal information’ by interacting with the environment itself, or it can collect ‘social information’ by observing the behaviour of others. The use of these two types of information varies across different situations and between individuals. Personality is a concept that captures consistent interindividual differences in behaviour and could be one of the factors driving interindividual variation in information use. We tested this by conducting behavioural experiments based on a colour association task in captive great tits, Parus major, originating from lines bidirectionally selected for high and low exploratory behaviour. We quantified personal information use by measuring to what extent a bird relied on previously rewarded options instead of novel options. Social information use was measured by recording how birds chose according to social information provided by video playbacks of a conspecific. Here, we demonstrate that variation in the use of both personal and social information is indeed personality related. In their decision making, slow explorers relied more on prior knowledge, from both personal and social origins, whereas fast explorers tended to ignore the available information and chose more randomly. The differences between the personality types imply different costs or constraints in acquiring and/or applying the two types of information, possibly due to variation in, for example, cognitive styles. In conclusion, we demonstrate that personality types have different strategies to cope with environmental uncertainty.
    https://doi.org/10.1016/j.anbehav.2019.02.002
  • Scientific data
    2019

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

    Hannu Mäkinen, Heidi 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
  • 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
  • Frontiers in Zoology
    2019

    Repeatability of signalling traits in the avian dawn chorus

    Marc Naguib, Joris Diehl, Kees van Oers, Lysanne Snijders
    Birdsong, a key model in animal communication studies, has been the focus of intensive research. Song traits are commonly considered to reflect differences in individual or territory quality. Yet, few studies have quantified the variability of song traits between versus within individuals (i.e. repeatability), and thus whether certain song traits indeed provide reliable individual-specific information. Here, we studied the dawn chorus of male great tits (Parus major) to determine if key song traits are repeatable over multiple days and during different breeding stages. Additionally, we examined whether repeatability was associated with exploration behaviour, a relevant personality trait. Finally, we tested if variation in song traits could be explained by breeding stage, lowest night temperature, and exploration behaviour.
    https://doi.org/10.1186/s12983-019-0328-7
  • 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
  • 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
  • Nature Ecology and Evolution
    2018

    Genomic tools for behavioral ecologists to understand repeatable individual differences in behavior

    Sarah Bengston, Romain Dahan, Zoe Donaldson, Steven Phelps, Kees van Oers, Andrew Sih, Alison Bell
    Behaviour is a key interface between an animal’s genome and its environment. Repeatable individual differences in behaviour have been extensively documented in animals, but the molecular underpinnings of behavioural variation among individuals within natural populations remain largely unknown. Here, we offer a critical review of when molecular techniques may yield new insights, and we provide specific guidance on how and whether the latest tools available are appropriate given different resources, system and organismal constraints, and experimental designs. Integrating molecular genetic techniques with other strategies to study the proximal causes of behaviour provides opportunities to expand rapidly into new avenues of exploration. Such endeavours will enable us to better understand how repeatable individual differences in behaviour have evolved, how they are expressed and how they can be maintained within natural populations of animals.
    https://doi.org/10.1038/s41559-017-0411-4
  • BMC Genomics
    2018

    CNVs are associated with genomic architecture in a songbird

    Vinicius Henrique da Silva, Veronika Laine, Mirte Bosse, Kees van Oers, B.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
  • Functional Ecology
    2018

    Maternal egg hormones in the mating context: the effect of pair personality

    Suvi Ruuskanen, T.G.G. Groothuis, A.T. Baugh, Sonja Schaper, B. de Vries, Kees van Oers
    Animal personality traits emerge developmentally from the interaction of genetic and early environmental factors. Maternal hormones, such as androgens (testosterone, T and androstenedione, A4), transferred to embryos and egg yolks may simultaneously organize multiple behavioural and physiological traits. Although previous studies demonstrated an association between the mother's personality and yolk androgen levels, the independent effects of the male partner's personality and pair combination remains unknown.
    We test this association using an ecological model species for personality research, the great tit (Parus major) using multiple approaches: (1) a wild population, (2) a randomly mated captive population and (3) an experimental study with (dis)assortatively mated pairs from lines selected for fast exploration/boldness or slow exploration/shyness.
    Egg androgen concentrations were associated with variation in female personality traits, and the experimental data suggested that this is independent of male personality: Experimental females from the slow-shy line tended to have higher egg T concentrations than females from the fast-bold line, with no effect of male personality. Shy females from the wild population had higher egg A4 concentration than bold females. However, in the correlative data yolk hormones were linked with male personality, as well as the interaction between female and male traits: Male handling responsiveness correlated negatively with egg A4 concentration in wild birds. In randomly mated birds, pairs that were mated assortatively for personality had lower egg T concentrations than disassortatively mated pairs.
    Given that egg androgens are known mediators of avian personality, our results suggest that maternal hormones might contribute to the heritability of personality, may be sensitive to the social context of mating, and act as key drivers of individual differences.
    https://doi.org/10.1111/1365-2435.12987
  • Journal of Evolutionary Biology
    2018

    Gene flow does not prevent personality and morphological differentiation between two blue tit populations

    G. Dubuc-Messier, Samuel P. Caro, C. Perrier, Kees van Oers, D. Réale, A. Charmantier
    Understanding the causes and consequences of population phenotypic divergence is a central goal in ecology and evolution. Phenotypic divergence among populations can result from genetic divergence, phenotypic plasticity or a combination of the two. However, few studies have deciphered these mechanisms for populations geographically close and connected by gene flow, especially in the case of personality traits. In this study, we used a common garden experiment to explore the genetic basis of the phenotypic divergence observed between two blue tit (Cyanistes caeruleus) populations inhabiting contrasting habitats separated by 25 km, for two personality traits (exploration speed and handling aggression), one physiological trait (heart rate during restraint) and two morphological traits (tarsus length and body mass). Blue tit nestlings were removed from their population and raised in a common garden for up to five years. We then compared adult phenotypes between the two populations, as well as trait‐specific Qst and Fst. Our results revealed differences between populations similar to those found in the wild, suggesting a genetic divergence for all traits. Qst ‐ Fst comparisons revealed that the traits divergences likely result from dissimilar selection patterns rather than from genetic drift. Our study is one of the first to report a Qst ‐ Fst comparison for personality traits and adds to the growing body of evidence that population genetic divergence is possible at a small scale for a variety of traits including behavioural traits.
    https://doi.org/10.1111/jeb.13291
  • 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
  • Journal of Experimental Biology
    2018

    SERT gene polymorphisms are associated with risk-taking behaviour and breeding parameters in wild great tits

    K. Timm, Kees van Oers, V. Tilgar
    Individual differences in coping with potentially dangerous situations are affected by a combination of genetic and environmental factors. How genetic polymorphisms and behavioural variations are related to fitness is unknown. One of the candidate genes affecting a variety of behavioural processes, including impulsivity, anxiety and mood fluctuations in both humans and other vertebrates is the serotonin transporter gene (SERT/SLC6A). The aim of this study was to assess an association between SERT genotypes and novelty seeking, risk-taking behaviours and breeding parameters of great tits (Parus major) in a natural environment. We associated polymorphisms in the promoter exonic regions of the SERT gene with parental risk-taking related behaviour and fitness traits. Our results show that (i) risk-taking behaviour in our great tit population is linked to single nucleotide polymorphisms in the SERT gene exon 3 and exon 8; (ii) the genotype-behaviour associations are consistent at the presence of different stressors; (iii) polymorphisms in exon 8 could be associated with fitness-related traits, such as the start of egg-laying and hatching success. We showed for the first time that genetic variability of SERT plays an important role in shaping individual decision-making that affects fitness consequences in a wild population. However, the results are based on one population and on the polymorphisms that are in one single gene. Therefore, replication studies are needed in order to confirm these preliminary results.
    https://doi.org/10.1242/jeb.171595
  • Journal of Animal Ecology
    2018

    Responses of insect herbivores and their food plants to wind exposure and the importance of predation risk.

    Cong Chen, Arjen Biere, R. Gols, W. Halfwerk, Kees van Oers, Jeff A. Harvey
    Wind is an important abiotic factor that influences an array of biological processes, but it is rarely considered in studies on plant–herbivore interactions.
    Here, we tested whether wind exposure could directly or indirectly affect the performance of two insect herbivores, Plutella xylostella and Pieris brassicae, feeding on Brassica nigra plants.
    In a greenhouse study using a factorial design, B. nigra plants were exposed to different wind regimes generated by fans before and after caterpillars were introduced on plants in an attempt to separate the effects of direct and indirect wind exposure on herbivores.
    Wind exposure delayed flowering, decreased plant height and increased leaf concentrations of amino acids and glucosinolates.
    Plant‐mediated effects of wind on herbivores, that is effects of exposure of plants to wind prior to herbivore feeding, were generally small. However, development time of both herbivores was extended and adult body mass of P. xylostella was reduced when they were directly exposed to wind. By contrast, wind‐exposed adult P. brassicae butterflies were significantly larger, revealing a trade‐off between development time and adult size.
    Based on these results, we conducted a behavioural experiment to study preference by an avian predator, the great tit (Parus major) for last instar P. brassicae caterpillars on plants that were exposed to either control (no wind) or wind (fan‐exposed) treatments. Tits captured significantly more caterpillars on still than on wind‐exposed plants.
    Our results suggest that P. brassicae caterpillars are able to perceive the abiotic environment and to trade off the costs of extended development time against the benefits of increased size depending on the perceived risk of predation mediated by wind exposure. Such adaptive phenotypic plasticity in insects has not yet been described in response to wind exposure.
    https://doi.org/10.1111/1365-2656.12835
  • 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
  • General and Comparative Endocrinology
    01-09-2017

    Temporal dynamics of the HPA axis linked to exploratory behavior in a wild European songbird (Parus major)

    Alexander T. Baugh, Sarah C. Davidson, Michaela Hau, Kees van Oers
    Abstract Variation in the reactivity of the endocrine stress axis is thought to underlie aspects of persistent individual differences in behavior (i.e. animal personality). Previous studies, however, have focused largely on estimating baseline or peak levels of glucocorticoids (CORT), often in captive animals. In contrast, the temporal dynamics of the HPA axis—how quickly it turns on and off, for example—may better indicate how an individual copes with stressors. Moreover, these HPA components might be correlated, thereby representing endocrine suites. Using wild-caught great tits (Parus major) we tested birds for exploratory behavior using a standardized novel environment assay that serves as a validated proxy for personality. We then re-captured a subset of these birds (n = 85) and characterized four components of HPA physiology: baseline, endogenous stress response, a dexamethasone (DEX) challenge to estimate the strength of negative feedback, and an adrenocorticotropic hormone (ACTH) challenge to estimate adrenal capacity. We predicted that these four HPA responses would be positively correlated and that less exploratory birds would have a more rapid onset of the stress response (a CORT elevation during the baseline bleed) and weaker negative feedback (higher CORT after DEX). We found support for the first two predictions but not the third. All four components were positively correlated with each other and less exploratory birds exhibited an elevation in CORT during the baseline bleed (<3 min from capture). Less exploratory birds, however, did not exhibit weaker negative feedback following the DEX challenge, but did exhibit weaker adrenal capacity. Together, our findings provide partial support for the hypothesis that the temporal reactivity of the HPA axis is linked with consistent individual differences in behavior, with more cautious (slower exploring) individuals exhibiting a faster CORT response.
    https://doi.org/10.1016/j.ygcen.2017.06.011
  • Journal of Avian Biology
    05-2017

    Context-dependent effects of radio transmitter attachment on a small passerine

    Lysanne Snijders, Lydia E. Nieuwe Weme, Piet De Goede, James L. Savage, Kees van Oers, Marc Naguib
    Biotelemetry devices provide unprecedented insights into the spatial behaviour and ecology of many animals. Quantifying the potential effects of attaching such devices to animals is essential, but certain effects may appear only in specific or particularly stressful contexts. Here we analyse the effects of radio tag attachment on great tits (Parus major) tagged over three environmentally dissimilar years, as part of a project studying social- and communication networks. When we radio-tagged birds before breeding, only those tagged in the coldest spring tended to be less likely to breed than control birds. Breeding probability was independent of the relative tag weight (between 5% and 8% bodyweight). When we radio-tagged both parents during nestling provisioning (tag weight between 6% and 8%), tagged parents were more likely than control parents to desert their brood in two of the three years, while in the other year no tagged parents deserted. Tagged parents provisioning larger broods were most likely to desert, especially during lower average temperatures. Video analyses did not reveal any tag effects on provisioning behaviour of parents in the year with no desertion. We conclude that radio tagging before breeding did not lead to negative effects, regardless of tag weight, but that decisions about radio-tagging parents during nestling provisioning need to be made with exceptional care, taking both environmental context and tag weight into account. Reporting results from long-term radio-tracking studies comprising several environmentally variable years is crucial to understand and predict potential tag effects and maximise the tremendous potential of biotelemetry.This article is protected by copyright. All rights reserved.
    https://doi.org/10.1111/jav.01148
  • Animal Behaviour
    2017

    Novelty induces behavioural and glucocorticoid responses in a songbird artificially selected for divergent personalities

    A.T. Baugh, K.R. Witonsky, S.C. Davidson, L. Hyder, M. Hau, Kees van Oers
    Stress physiology is thought to contribute to individual differences in behaviour. In part this reflects the fact that canonical personality measures consist of responses to challenges, including novel objects and environments. Exposure to novelty is typically assumed to induce a moderate increase in glucocorticoids (CORT), although this has rarely been tested. We tested this assumption using great tits, Parus major, selected for divergent personalities (bold-fast and shy-slow explorers), predicting that the shy birds would exhibit higher CORT following exposure to a novel object. We also scored behavioural responses to the novel object, predicting that bold birds would more frequently approach the novel object and exhibit more abnormal repetitive behaviours. We found that the presence of a novel object did induce a moderate CORT response, but selection lines did not differ in the magnitude of this response. Furthermore, although both selection lines showed a robust CORT elevation to a subsequent restraint stressor, the CORT response was stronger in bold birds and this effect was specific to novel object exposure. Shy birds showed a strong positive phenotypic correlation between CORT concentrations following the novel object exposure and the subsequent restraint stress. Behaviourally, the selection lines differed in their response during novel object exposure: as predicted, bold birds more frequently approached the novel object and shy birds more strongly decreased overall locomotion during the novel object trial, but birds from both selection lines showed significant and similar frequencies of abnormal repetitive behaviours during novel object exposure. Our findings support the hypothesis that personality emerges as a result of correlated selection on behaviour and underlying endocrine mechanisms and suggest that the relationship between endocrine stress physiology and personality is context dependent.
    https://doi.org/10.1016/j.anbehav.2017.06.028
  • Hormones and Behavior
    2017

    Risk-averse personalities have a systemically potentiated neuroendocrine stress axis: a multilevel experiment in Parus major

    A.T. Baugh, R.A. Senft, M. Firke, A. Lauder, J. Schroeder, S.L. Meddle, Kees van Oers, Michaela Hau
    Hormonal pleiotropy—the simultaneous influence of a single hormone on multiple traits—has been hypothesized as an important mechanism underlying personality, and circulating glucocorticoids are central to this idea. A major gap in our understanding is the neural basis for this link. Here we examine the stability and structure of behavioral, endocrine and neuroendocrine traits in a population of songbirds (Parus major). Upon identifying stable and covarying behavioral and endocrine traits, we test the hypothesis that risk-averse personalities exhibit a neuroendocrine stress axis that is systemically potentiated—characterized by stronger glucocorticoid reactivity and weaker negative feedback. We show high among-individual variation and covariation (i.e. personality) in risk-taking behaviors and demonstrate that four aspects of glucocorticoid physiology (baseline, stress response, negative feedback strength and adrenal sensitivity) are also repeatable and covary. Further, we establish that high expression of mineralocorticoid and low expression of glucocorticoid receptor in the brain are linked with systemically elevated plasma glucocorticoid levels and more risk-averse personalities. Our findings support the hypothesis that steroid hormones can exert pleiotropic effects that organize behavioral phenotypes and provide novel evidence that neuroendocrine factors robustly explain a large fraction of endocrine and personality variation.
    https://doi.org/10.1016/j.yhbeh.2017.05.011
  • Ecology and Evolution
    2017

    Sex-specific responses to territorial intrusions in a communication network: evidence from radio-tagged great tits

    Lysanne Snijders, Kees van Oers, Marc Naguib
    Signals play a key role in the ecology and evolution of animal populations, influencing processes such as sexual selection and conflict resolution. In many species, sexually selected signals have a dual function: attracting mates and repelling rivals. Yet, to what extent males and females under natural conditions differentially respond to such signals remains poorly understood, due to a lack of field studies that simultaneously track both sexes. Using a novel spatial tracking system, we tested whether or not the spatial behavior of male and female great tits (Parus major) changes in relation to the vocal response of a territorial male neighbor to an intruder. We tracked the spatial behavior of male and female great tits (N = 44), 1 hr before and 1 hr after simulating territory intrusions, employing automatized Encounternet radio-tracking technology. We recorded the spatial and vocal response of the challenged males and quantified attraction and repulsion of neighboring males and females to the intrusion site. We additionally quantified the direct proximity network of the challenged male. The strength of a male's vocal response to an intruder induced sex-dependent movements in the neighborhood, via female attraction and male repulsion. Stronger vocal responders were older and in better body condition. The proximity networks of the male vocal responders, including the number of sex-dependent connections and average time spent with connections, however, did not change directly following the intrusion. The effects on neighbor movements suggest that the strength of a male's vocal response can provide relevant social information to both the males and the females in the neighborhood, resulting in both sexes adjusting their spatial behavior in contrasting ways, while the social proximity network remained stable. This study underlines the importance of “silent” eavesdroppers within communication networks for studying the dual functioning and evolution of sexually selected signals.
    https://doi.org/10.1002/ece3.2686
  • Ecology Letters
    2017

    Direct fitness benefits explain mate preference, but not choice, for similarity in heterozygosity levels

    Lies Zandberg, G. Gort, Kees van Oers, C.A. Hinde
    Under sexual selection, mate preferences can evolve for traits advertising fitness benefits. Observed mating patterns (mate choice) are often assumed to represent preference, even though they result from the interaction between preference, sampling strategy and environmental factors. Correlating fitness with mate choice instead of preference will therefore lead to confounded conclusions about the role of preference in sexual selection. Here we show that direct fitness benefits underlie mate preferences for genetic characteristics in a unique experiment on wild great tits. In repeated mate preference tests, both sexes preferred mates that had similar heterozygosity levels to themselves, and not those with which they would optimise offspring heterozygosity. In a subsequent field experiment where we cross fostered offspring, foster parents with more similar heterozygosity levels had higher reproductive success, despite the absence of assortative mating patterns. These results support the idea that selection for preference persists despite constraints on mate choice.
    https://doi.org/10.1111/ele.12827
  • Scientific Reports
    2017

    Inefficient co-feeding transmission of Borrelia afzelii in two common European songbirds

    D.J.A. Heylen, H. Sprong, A. Krawczyk, N. Van Houtte, D. Genné, A. Gomez-Chamorro, Kees van Oers, Maarten J. Voordouw
    The spirochete bacterium Borrelia afzelii is the most common cause of Lyme borreliosis in Europe. This tick-borne pathogen can establish systemic infections in rodents but not in birds. However, several field studies have recovered larval Ixodes ricinus ticks infected with B. afzelii from songbirds suggesting successful transmission of B. afzelii. We reviewed the literature to determine which songbird species were the most frequent carriers of B. afzelii-infected I. ricinus larvae and nymphs. We tested experimentally whether B. afzelii is capable of co-feeding transmission on two common European bird species, the blackbird (Turdus merula) and the great tit (Parus major). For each bird species, four naïve individuals were infested with B. afzelii-infected I. ricinus nymphal ticks and pathogen-free larval ticks. None of the co-feeding larvae tested positive for B. afzelii in blackbirds, but a low percentage of infected larvae (3.33%) was observed in great tits. Transstadial transmission of B. afzelii DNA from the engorged nymphs to the adult ticks was observed in both bird species. However, BSK culture found that these spirochetes were not viable. Our study suggests that co-feeding transmission of B. afzelii is not efficient in these two songbird species.
    https://doi.org/10.1038/srep39596
  • Behavioural Processes
    2017

    Personality-dependent differences in problem-solving performance in a social context reflect foraging strategies

    Lies Zandberg, John L. Quinn, Marc Naguib, Kees van Oers
    Abstract Individuals develop innovative behaviours to solve foraging challenges in the face of changing environmental conditions. Little is known about how individuals differ in their tendency to solve problems and in their subsequent use of this solving behaviour in social contexts. Here we investigated whether individual variation in problem-solving performance could be explained by differences in the likelihood of solving the task, or if they reflect differences in foraging strategy. We tested this by studying the use of a novel foraging skill in groups of great tits (Parus major), consisting of three naive individuals with different personality, and one knowledgeable tutor. We presented them with multiple, identical foraging devices over eight trials. Though birds of different personality type did not differ in solving latency; fast and slow explorers showed a steeper increase over time in their solving rate, compared to intermediate explorers. Despite equal solving potential, personality influenced the subsequent use of the skill, as well as the pay-off received from solving. Thus, variation in the tendency to solve the task reflected differences in foraging strategy among individuals linked to their personality. These results emphasize the importance of considering the social context to fully understand the implications of learning novel skills.
    https://doi.org/10.1016/j.beproc.2016.09.007
  • Behavioral Ecology
    2017

    Dominance rank and boldness predict social attraction in great tits

    Lysanne Snijders, Marc Naguib, Kees van Oers
    Social relationships can have important fitness consequences, and how well an individual is socially connected often correlates with other behavioral traits. Whether such correlations are caused by underlying individual differences in social attraction usually remains unclear, because to identify effects of individual traits on social attraction, it is essential to experimentally exclude the influence of the social partner. Using standardized high-definition video playback on captive great tits (Parus major), we effectively demonstrate the influence of individual traits on the motivation to be near a conspecific. We show that social attraction varied contrastingly with boldness and stimulus novelty. Shyer birds tended to show stronger social attraction when they were confronted with the stimulus bird for the first time. Lower ranked birds showed the overall strongest social attraction. This rank effect remained after experimentally changing dominance ranks by altering group compositions. Moreover, preference for social association tended to increase with a decrease in dominance rank, suggesting that birds plastically change their social preference in relation to their within-group dominance status. Our results provide insight into how social relations can form and change, processes that are key for understanding the long-term consequences of the social environment, and the role individuals might play in influencing this environment themselves.
    https://doi.org/10.1093/beheco/arw158
  • 2017

    The Quantitative and Molecular Genetics of Individual Differences in Animal Personality

    Veronika Laine, Kees van Oers
    One of the main goals in current personality research is to identify genes behind the measured behavioral variations. This is important in order to study how, under the influence of the environment, gene expression changes are translated into the observed phenotypes. The advances, especially in genomic technologies, have made it possible to identify genetic loci behind these variations, also concerning non-model species. In this chapter, we will describe the role and relevance of quantitative and molecular genetic approaches in explaining the existence and maintenance of variation in animal personality. We here will provide (1) a timely review on the papers published on this topic, (2) an overview of the current situation and progress, and (3) a view on the likely new avenues the field will take.
    https://doi.org/10.1007/978-3-319-59300-5_4
  • Trends in Ecology & Evolution
    07-2016

    Bolder Takes All and the role of epigenetics. A comment on Canestrelli et al.

    Marleen Cobben, Kees van Oers
    Refers To Daniele Canestrelli, Roberta Bisconti, Claudio Carere Bolder Takes All? The Behavioral Dimension of Biogeography Trends in Ecology & Evolution, Volume 31, Issue 1, January 2016, Pages 35-43 PDF (1863 K)
    https://doi.org/10.1016/j.tree.2016.04.007
  • 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, M. Cichoń, T. Eeva, A. Grégoire, C.A. Hinde, A. Johnsen, J. Komdeur, R. Mänd, E. Matthysen, A.C. Norte, N. Pitala, Ben C. Sheldon, T. Slagsvold, J.M. Tinbergen, J. Török, R. Ubels, Kees van Oers, Marcel E. Visser, Blandine 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
  • Behavioral Ecology
    05-2016

    To sing or not to sing: seasonal changes in singing vary with personality in wild great tits

    Marc Naguib, E.P. van Rooij, Lysanne Snijders, Kees van Oers
    Expression of sexually selected signals in many species varies over time of day and season. A key model system to study this variation in signal expression is birdsong. Yet, despite good ecological understanding of why song varies across time of day and season, much of the individual variation remains unexplained. Although some of the interindividual variation in singing depends on the quality or motivation of an individual, it can also vary with other characteristics. Because singing has been shown to vary with personality traits in specific contexts, personality is thus an important candidate to explain part of the variation in seasonal and daily singing. Using a personality-typed field population of great tits (Parus major), we here show that singing activity peaked at dawn during the fertile period of the females and that the association between male personality and singing activity depended on the reproductive stage of his mate; faster explorers significantly increased in singing activity during main periods of fertility and maternal investment (egg laying and incubation). Moreover, males with higher singing activity tended to raise more fledglings. Increased singing by faster explorers during key periods of female reproductive investment suggests that faster explorers are more responsive to changes in female reproductive stage, contrasting the general view that faster explorers are less responsive to environmental and social changes. Most importantly, these findings highlight that multiple factors including personality need to be integrated when assessing causes of variation of highly variable sexually selected signal traits.
    https://doi.org/10.1093/beheco/arv235
  • BMC Genomics
    2016

    Gene and transposable element methylation in great tit (Parus major) brain and blood

    Martijn Derks, K.M. Schachtschneider, Ole Madsen, Elio GWM Schijlen, Koen Verhoeven, Kees van Oers

    Background

    Studies on vertebrate DNA methylomes have revealed a regulatory role of tissue specific DNA methylation in relation to gene expression. However, it is not well known how tissue-specific methylation varies between different functional and structural components of genes and genomes. Using whole-genome bisulfite sequencing data we here describe both CpG and non-CpG methylation profiles of whole blood and brain tissue in relation to gene features, CpG-islands (CGIs), transposable elements (TE), and their functional roles in an ecological model species, the great tit (Parus major).


    Results

    We show that hypomethylation at the transcription start site (TSS) is enriched in genes with functional classes that relate directly to processes specific to each tissue type. We find that 6877 (~21 %) of the CGIs are differentially methylated between blood and brain, of which 1186 and 2055 are annotated to promoter and intragenic regions, respectively. We observe that CGI methylation in promoter regions is more conserved between tissues compared to CGI methylation in intra and inter-genic regions. Differentially methylated CGIs in promoter and intragenic regions are overrepresented in genomic loci linked to development, suggesting a distinct role for CGI methylation in regulating expression during development. Additionally, we find significant non-CpG methylation in brain but not in blood with a strong preference for methylation at CpA dinucleotide sites. Finally, CpG hypermethylation of TEs is significantly stronger in brain compared to blood, but does not correlate with TE activity. Surprisingly, TEs showed significant hypomethylation in non-CpG contexts which was negatively correlated with TE expression.


    Conclusion

    The discovery that TSS methylation levels are directly linked to functional classes related to each tissue provides new insights in the regulatory role of DNA-methylation patterns. The dominant sequence motifs for brain non-CpG methylation, similar to those found in mammals, suggests that a conserved non-CpG regulatory mechanism was already present in the amniote ancestor. The negative correlation between brain non-CpG methylation and TE activity (not found for CpG methylation) suggests that non-CpG is the dominant regulatory form of methylation in TE silencing.
    https://doi.org/10.1186/s12864-016-2653-y
  • 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
  • General and Comparative Endocrinology
    2016

    Effects of experimentally sustained elevated testosterone on incubation behaviour and reproductive success in female great tits (Parus major).

    B. de Jong, L. Lens, S.M. Amininasab, Kees van Oers, V.M. Darras, M. Eens, R. Pinxten, J. Komdeur, T.G.G. Groothuis
    n many seasonally breeding birds, female and male testosterone (T) levels peak at the start of the breeding season, coinciding with pair bonding and nesting activities. Shortly after the onset of egg laying, T levels slowly decline to baseline levels in both sexes, but more rapidly so in females. During this period, T in males may still function to facilitate territorial behaviour, mate guarding and extra pair copulations, either via short lasting peaks or elevated basal levels of the hormone. In some species, however, males become insensitive to increased T after the onset of egg laying. It has been postulated that in these species bi-parental care is essential for offspring survival, as T is known to inhibit paternal care. However, only very few studies have analysed this for females. As females are heavily involved in parental care, they too might become insensitive to T after egg laying. Alternatively, because territorial defence, mate guarding and extra pair copulations are expected to be less important for females than for males, they may not have had the need to evolve a mechanism to become insensitive to T during the period of maternal care, because their natural T levels are never elevated during this part of the breeding season anyway. We tested these alternative hypotheses in female great tits (Parus major). Male great tits have previously been shown to be insensitive to T after egg laying with regard to nestling feeding behaviour (but not song rate). When females had started nest building, we experimentally elevated their T levels up to the nestling feeding phase, and measured incubation behaviour (only females incubate) and reproductive success. T did not significantly affect nest building or egg laying behaviour, although egg laying tended to be delayed in T females. Females with experimentally enhanced T maintained lower temperature during incubation but did not spend less time incubating. This might explain the reduced hatching success of their eggs, smaller brood size and lower number of fledglings we found in this study. As in this species T-dependent behaviour by females during the phase of parental care is not needed, the results support the hypothesis that in this species the need for selection in favour of T-insensitivity did not occur.
    https://doi.org/10.1016/j.ygcen.2016.02.017
  • Nature Communications
    2016

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

    Veronika Laine, T.I. Gossmann, K.M. Schachtschneider, C.J. Garroway, O. Madsen, Koen Verhoeven, Victor de Jager, H-J. Megens, W.C. Warren, P. Minx, R.P.M.A. Crooijmans, P. Corcoran, Ben C. Sheldon, J. Slate, K. 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
  • Molecular Ecology
    2016

    Evidence from Pyrosequencing Indicates that Natural Variation in Animal Personality is Associated with DRD4 DNA Methylation

    Eveline Verhulst, A.C. Mateman, M.V. Zwier, Samuel P. Caro, Koen Verhoeven, Kees van Oers
    Personality traits are heritable and respond to natural selection, but are at the same time influenced by the ontogenetic environment. Epigenetic effects, such as DNA methylation, have been proposed as a key mechanism to control personality variation. However, to date little is known about the contribution of epigenetic effects to natural variation in behaviour. Here, we show that great tit (Parus major) lines artificially selected for divergent exploratory behaviour for four generations differ in their DNA methylation levels at the dopamine receptor D4 (DRD4) gene. This D4 receptor is statistically associated with personality traits in both humans and nonhuman animals, including the great tit. Previous work in this songbird failed to detect functional genetic polymorphisms within DRD4 that could account for the gene–trait association. However, our observation supports the idea that DRD4 is functionally involved in exploratory behaviour but that its effects are mediated by DNA methylation. While the exact mechanism underlying the transgenerational consistency of DRD4 methylation remains to be elucidated, this study shows that epigenetic mechanisms are involved in shaping natural variation in personality traits. We outline how this first finding provides a basis for investigating the epigenetic contribution to personality traits in natural systems and its subsequent role for understanding the ecology and evolution of behavioural consistency.
    https://doi.org/10.1111/mec.13519
  • Molecular Ecology
    12-2015

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

    A.W. Santure, J. 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
  • Frontiers in Zoology
    2015

    Parental food provisioning is related to nestling stress response in wild great tit nestlings: implications for the development of personality

    Kees van Oers, G.M. Kohn, C.A. Hinde, Marc Naguib
    Background
    Variation in early nutrition is known to play an important role in shaping the behavioural development of individuals. Parental prey selection may have long-lasting behavioural influences. In birds foraging on arthropods, for instance, the specific prey types, e.g. spiders and caterpillars, matter as they have different levels of taurine which may have an effect on personality development. Here we investigated how naturally occurring variation in the amounts of spiders and caterpillars, provisioned to nestlings at day 4 and 8 after hatching, is related to the response to handling stress in a wild passerine, the great tit (Parus major). Broods were cross-fostered in a split-brood design allowing us to separate maternal and genetic effects from early rearing effects. Adult provisioning behaviour was monitored on day four and day eight after hatching using video recordings. Individual nestlings were subjected to a handling stress test at an age of 14 days, which is a validated proxy for exploratory behaviour as an adult.

    Results
    Variation in handling stress was mainly determined by the rearing environment. We show that, contrary to our predictions, not the amount of spider biomass, but the amount of caterpillar biomass delivered per nestling significantly affected individual performance in the stress test. Chicks provisioned with lower amounts of caterpillars exhibited a stronger stress response, reflecting faster exploratory behaviour later on in life, than individuals who received larger amounts of caterpillars.

    Conclusions
    These results suggest that natural variation in parental behaviour in wild birds modulates the developmental trajectories of their offspring's personality via food provisioning. Since parental provisioning behaviour might also reflect the local environmental conditions, provisioning behaviour may influence how nestlings respond to these local environmental conditions.
    https://doi.org/10.1186/1742-9994-12-S1-S10
  • PLoS One
    2015

    Song Trait Similarity in Great Tits Varies with Social Structure

    Lysanne Snijders, Jerine van der Eijk, Erica P. van Rooij, Piet De Goede, Kees van Oers, Marc Naguib
    https://doi.org/10.1371/journal.pone.0116881
  • Animal Behaviour
    2015

    Dawn song predicts behaviour during territory conflicts in personality-typed great tits

    Lysanne Snijders, E.P. van Rooij, M.F.A. Henskens, Kees van Oers, Marc Naguib
    Territorial animals settle territory disputes and discourage conspecific intrusion via close-range confrontations as well as nonconfrontational long-range signalling. Since individuals often differ consistently in general aggression and risk taking, the relative use of either close- or long-range territorial defence behaviour is likely to vary with the personality of the territory owner. Here we quantified the relationship between dawn song, a well-studied long-range signal, and responses to a close-range confrontation as well as how individuals in a territorial population vary in this relationship. For this we recorded dawn song and experimentally simulated territory intrusions via playbacks in wild personality-typed male great tits, Parus major. We show that males that sang at a higher rate at dawn also showed stronger vocal responses towards a simulated intruder, but spent less time in proximity to the intruder. Moreover, males with a higher exploration score, an established proxy for personality traits, showed the strongest vocal and spatial responses during the confrontation, yet exploration behaviour did not predict the dawn song rate. These findings highlight the importance of both confrontational and nonconfrontational territorial behaviours as well as personality for the social and territorial dynamics of animal populations.
    https://doi.org/10.1016/j.anbehav.2015.07.037
  • Functional Ecology
    2015

    Costs of sleeping in: circadian rhythms influence cuckoldry risk in a songbird

    Timothy J. Greives, Sjouke A. kingma, Bart Kranstauber, Kim G. Mortega, Martin Wikelski, Kees van Oers, A.C. Mateman, Glen A. Ferguson, Giulia Beltrami, M. Hau
    Circadian (i.e. daily) regulation of behaviors is thought to provide fitness benefits to organisms by enabling them to anticipate diel changes in the environment, such as sunrise. A common behavior among socially monogamous songbirds that usually takes place in the early mornings is copulating with partners outside of the social pair bond (i.e., extra-pair mating). Thus, variation in when individuals begin their daily activity may influence their reproductive success; early risers may be better able to gain copulations and be able to guard their partners and minimize their risk of being cuckolded compared to late risers. Sexual selection may thus play an important role in shaping circadian behaviors, but this assumption has yet to be tested in free-living animals. Here we experimentally weakened endogenous circadian rhythmicity and thus anticipation of dawn in male great tits (Parus major) in the wild through the subcutaneous administration of an implants filled with melatonin shortly before egg-laying began in this population. Selection, particularly sexual selection, may shape circadian phenotypes of wild vertebrates which enable anticipation of important and predictive diel changes in an individuals biotic and abiotic environment.
    https://doi.org/10.1111/1365-2435.12440
  • PLoS One
    2015

    Gender and personality differences in response to social stressors in great tits (Parus major)

    E. van der Meer, Kees van Oers
    In response to stressors, animals can increase the activity of the hypothalamic-pituitary-adrenocortical axis, resulting in elevated glucocorticoid concentrations. An increase in glucocorticoids results in an increase in heterophils and a decrease in lymphocytes, which ratio (H/L-ratio) is an indicator of stress in birds. The physiological response to a stressor can depend on individual characteristics, like dominance rank, sex and personality. Although the isolated effects of these characteristics on the response to a stressor have been well studied, little is known about the response in relation to a combination of these characteristics. In this study we investigate the relationship between social stress, dominance rank, sex and exploratory behaviour as a validated operational measure of personality in great tits (Parus major). Great tits show consistent individual differences in behaviour and physiology in response to stressors, and exploratory behaviour can be classified as fast or slow exploring. We group-housed four birds, two fast and two slow explorers, of the same sex that were previously singly housed, in an aviary and compared the H/L-ratio, lymphocyte and heterophil count before and after group housing. After experiencing the social context all birds increased their H/L-ratio and heterophil count. Females showed a stronger increase in H/L-ratio and heterophil count than males, which seemed to be related to a higher number of agonistic interactions compared to males. Dominance rank and exploration type did not affect the H/L-ratio or heterophil count. Contrary to our expectations, all birds increased their lymphocyte count. However, this increase was slower for fast than for slow explorers. Our study suggests that personality and sex related differences, but not dominance rank, are associated with changes in an individual's physiological response due to a social context.
    https://doi.org/10.1371/journal.pone.0127984
  • General and Comparative Endocrinology
    2014

    Baseline and stress-induced glucocorticoid concentrations are not repeatable but covary within individual great tits (Parus major)

    A.T. Baugh, Kees van Oers, N.J. Dingemanse, M. Hau
    In evolutionary endocrinology, there is a growing interest in the extent and basis of individual variation in endocrine traits, especially circulating concentrations of hormones. This is important because if targeted by selection, such individual differences present the opportunity for an evolutionary response to selection. It is therefore necessary to examine whether hormone traits are repeatable in natural populations. However, research in this area is complicated by the fact that different hormone traits can be correlated. The nature of these trait correlations (i.e., phenotypic, within-, or among-individual) is critically relevant in terms of the evolutionary implications, and these in turn, depend on the repeatability of each hormone trait. By decomposing phenotypic correlations between hormone traits into their within- and among-individual components it is possible to describe the multivariate nature of endocrine traits and generate inferences about their evolution. In the present study, we repeatedly captured individual great tits (Parus major) from a wild population and measured plasma concentrations of corticosterone. Using a mixed-modeling approach, we estimated repeatabilities in both initial (cf. baseline; CORT0) and stress-induced concentrations (CORT30) and the correlations between those traits among- and within-individuals. We found a lack of repeatability in both CORT0 and CORT30. Moreover, we found a strong phenotypic correlation between CORT0 and CORT30, and due to the lack of repeatability for both traits, there was no among-individual correlation between these two traits—i.e., an individual’s average concentration of CORT0 was not correlated with its average concentration of CORT30. Instead, the phenotypic correlation was the result of a strong within-individual correlation, which implies that an underlying environmental factor co-modulates changes in initial and stress-induced concentrations within the same individual over time. These results demonstrate that (i) a phenotypic correlation between two hormone traits does not imply that the traits are correlated among individuals; (ii) the importance of repeated sampling to partition within- and among-individual variances and correlations among labile physiological traits; and (iii) that environmental factors explain a considerable fraction of the variation and co-variation in hormone concentrations.
    https://doi.org/10.1016/j.ygcen.2014.08.014
  • 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
  • Environmental Microbiology
    2014

    Are the specialized bird ticks, Ixodes arboricola and I. frontalis, competent vectors for Borrelia burgdorferi sensu lato?

    D. Heylen, H. Sprong, Kees van Oers, M. Fonville, E. Matthysen
    Our study tested whether two European bird-specialized ticks, Ixodes arboricola and I. frontalis, can act as vectors in the transmission cycles of Borrelia burgdorferi s.l. The ticks have contrasting ecologies but share songbird hosts (such as the great tit, Parus major) with the generalist I. ricinus which may therefore act as a bridging vector. In the first phase of the experiment, we obtained Borrelia-infected ornithophilic nymphs by exposing larvae to great tits that had previously been exposed to I. ricinus nymphs carrying a community of genospecies (Borrelia garinii, valaisiana, afzelii, burgdorferi s.s., spielmanii). Skin samples showed that birds selectively amplified B. garinii and B. valaisiana. The spirochetes were transmitted to the ornithophilic ticks and survived moulting, leading to infection rates of 16% and 27% in nymphs of I. arboricola and I. frontalis respectively. In the second phase, pathogen-free great tits were exposed to the Borrelia-infected ornithophilic nymphs. None of these ticks were able to infect the birds, as indicated by the tissue samples. Analysis of xenodiagnostic I. ricinus larvae found no evidence for co-feeding or systemic transmission of B. burgdorferi s.l. These outcomes do not support the occurrence of enzootic cycles of Borrelia burgdorferi s.l. involving songbirds and their specialized ornithophilic ticks.
    https://doi.org/10.1111/1462-2920.12332
  • 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
  • Animal Behaviour
    2014

    Becoming more like your mate: hormonal similarity reduces divorce rates in a wild songbird

    Jenny Ouyang, Kees van Oers, M. Quetting, M. Hau
    In animals with biparental care, maintaining a pair bond is of adaptive value because it increases reproductive success and reduces costs, such as energy and time, for finding a new mate. Hormones are important mediators of social behaviours as well as parental care, and endocrine mechanisms are therefore likely to be involved in the decision whether to stay with the same mate or separate after a breeding season. Because behavioural compatibility has been shown to increase fitness and hormones have been shown to regulate behavioural traits, here we examined whether the degree of endocrine similarity is also related to reproductive success and pair bond longevity. We used a 3-year study on free-living great tits, Parus major, to test whether mates had similar hormone levels during the parental phase. We tested specifically whether the metabolic hormone corticosterone was related to pair bond longevity and reproductive success. Baseline, but not stress-induced, corticosterone concentrations were highly correlated among members of a pair and became more similar among members of pairs that stayed together for multiple years. Pairs that increased their hormonal similarity within a season (from prebreeding to breeding) had the highest reproductive success. Pairs with more similar baseline corticosterone levels and higher reproductive success were also more likely to remain together after the breeding season. The results of this study suggest that pair bond longevity is related to endocrine similarity and reproductive success, and raise the possibility that hormonal mechanisms may be under sexual selection.
    https://doi.org/10.1016/j.anbehav.2014.09.032
  • General and Comparative Endocrinology
    2013

    Initial reactivity and magnitude of the acute stress response associated with personality in wild great tits (Parus major)

    A.T. Baugh, Kees van Oers, Marc Naguib, M. Hau
    Phenotypic correlations, such as those between functionally distinct behavioral traits, can emerge through the action of selection on individual traits, on trait combinations, and through pleiotropic mechanisms. Steroid hormones are known to have pleiotropic effects on a suite of behavioral and physiological traits, including stable individual differences in coping with stress. Characterizing the stress axis in relation to personality, however, has typically focused on estimating baseline and peak levels of glucocorticoids, principally in captive animals. In contrast, the reactivity of the stress response—how quickly it turns on and persists—may better indicate the ability of an individual to cope with challenges, particularly in free-living animals. Using wild great tits (Parus major) we tested the hypothesis that cautious individuals respond to a standardized stressor with a more reactive stress response compared to bolder individuals. Wild birds were captured and tested for exploration behavior in a novel environment—an operational measure of personality in this species—and assessed separately for their glucocorticoid response to a standardized stressor. Slower explorers exhibited a greater elevation in glucocorticoid levels within the first three minutes after capture. Further, slower explorers reached a higher maximum CORT concentration and had higher total exposure to glucocorticoids during the stressor period. These data provide evidence that the temporal reactivity of the endocrine stress response, specifically its speed and magnitude, is associated with stable behavioral traits in free-living animals. Keywords Corticosterone; Exploration; Hypothalamic–pituitary–adrenal axis; Personality; Stress reactivity
    https://doi.org/10.1016/j.ygcen.2013.04.030
  • Ardea
    2013

    GAPDH as a control gene to estimate genome copy number in Great Tits, with cross-amplification in Blue Tits

    Els Atema, Kees van Oers, S. Verhulst
    Estimating the number of genome copies in a tissue sample can serve various purposes. For example, such an estimate serves as scaling variable when measuring telomeres with quantitative PCR. We describe the primer development and evaluation for the glyceraldehyde-3-phosphate dehydrogenase (GAPDH) gene in the Great Tit Parus major, as a control gene to estimate genome copy number. We demonstrate specific amplification with negligible variation in 48 Great Tits and cross-amplification in 53 Blue Tits Cyanistes caeruleus. We conclude this primer set to be reliable for amplification of GAPDH as a reference gene for quantitative PCR analysis in Great and Blue Tits.
    https://doi.org/10.5253/078.101.0107
  • Animal Behaviour
    2013

    Noise annoys: effects of noise on breeding great tits depend on personality but not on noise characteristics

    Marc Naguib, Kees van Oers, A. Braakhuis, M. Griffioen, Piet De Goede, J.R. Waas
    Anthropogenic noise can have serious implications for animals, especially when they communicate acoustically. Yet, the impacts of noise may depend not only on noise characteristics but also on an individual's coping style or personality. We tested whether noise is more disturbing if it masks communication signals, and whether characteristics of both the noise and the individual affect its impact. Using a unique population of personality-typed great tits, Parus major, we tested whether the kind of noise and parental personality affect parental nestbox visits and nestling begging. Nestboxes were exposed to automated noise playbacks, differing in spectral composition (noise masking begging calls, nonmasking noise or no noise). Parental nestbox visits were recorded using RFID transponders. Video and audio recordings were used to quantify nestling begging. Nestlings mainly begged in silence and in the presence of parents. Parents reduced nestbox visits during noise treatments regardless of the kind of noise and initially reacted more strongly to nonmasking noise. Moreover, slower explorers took longer to enter the nestbox during noise than faster explorers. Total visit rates during noise depended on parental sex and personality. In females, bolder individuals, but in males shyer individuals, reduced total visits during noise. These results extend previous findings in showing experimentally that the disturbance effects of noise do not depend on whether or not the noise directly interferes with information exchange by masking signals. Moreover, personality- and sex-specific responses to noise indicate that anthropogenic disturbance can differentially affect individuals within populations, which will influence mitigation strategies.
    https://doi.org/10.1016/j.anbehav.2013.02.015
  • Molecular Ecology
    2013

    Haplotype structure, adaptive history and associations with exploratory behaviour of the DRD4 gene region in four great tit (Parus major) populations

    J.C. Mueller, P. Korsten, C. Hermannstädter, T. Fuelner, N.J. Dingemanse, E. Matthysen, Kees van Oers, T. van Overveld, S.C. Patrick, J.L. Quinn, M. Riemenschneider, J. Tinbergen, B. Kempenaers
    The assessment of genetic architecture and selection history in genes for behavioural traits is fundamental to our understanding of how these traits evolve. The dopamine receptor D4 (DRD4) gene is a prime candidate for explaining genetic variation in novelty seeking behaviour, a commonly assayed personality trait in animals. Previously, we showed that a single nucleotide polymorphism in exon 3 of this gene is associated with exploratory behaviour in at least one of four Western European great tit (Parus major) populations. These heterogeneous association results were explained by potential variable linkage disequilibrium (LD) patterns between this marker and the causal variant or by other genetic or environmental differences among the populations. Different adaptive histories are further hypothesized to have contributed to these population differences. Here, we genotyped 98 polymorphisms of the complete DRD4 gene including the flanking regions for 595 individuals of the four populations. We show that the LD structure, specifically around the original exon 3 SNP is conserved across the four populations and does not explain the heterogeneous association results. Study-wide significant associations with exploratory behaviour were detected in more than one haplotype block around exon 2, 3 and 4 in two of the four tested populations with different allele effect models. This indicates genetic heterogeneity in the association between multiple DRD4 polymorphisms and exploratory behaviour across populations. The association signals were in or close to regions with signatures of positive selection. We therefore hypothesize that variation in exploratory and other dopamine-related behaviour evolves locally by occasional adaptive shifts in the frequency of underlying genetic variants.
    https://doi.org/10.1111/mec.12282
  • 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, B.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
  • Animal Cognition
    2012

    Worms under cover: relationship between performance in learning tasks and personality in great tits (Parus major)

    Mathieu Amy, Kees van Oers, Marc Naguib
    In animals, individual differences in learning ability are common and are in part explained by genetic differences, developmental conditions and by general experience. Yet, not all variations in learning are well understood. Individual differences in learning may be associated with elementary individual characteristics that are consistent across situations and over time, commonly referred to as personality or temperament. Here, we tested whether or not male great tits (Parus major) from two selection lines for fast or slow exploratory behaviour, an operational measure for avian personality, vary in their learning performance in two related consecutive tasks. In the first task, birds had to associate a colour with a reward whereas in the second task, they had to associate a new colour with a reward ignoring the previously rewarded colour. Slow explorers had shorter latencies to approach the experimental device compared with fast explorers in both tasks, but birds from the two selection lines did not differ in accomplishing the first task, that is, to associate a colour with a reward. However, in the second task, fast explorers had longer latencies to solve the trials than slow explorers. Moreover, relative to the number of trials needed to reach the learning criteria in the first task, birds from the slow selection line took more trials to associate a new colour with a reward while ignoring the previously learned association compared with birds from the fast selection line. Overall, the experiments suggest that personality in great tits is not strongly related to learning per se in such an association task, but that birds from different selection lines might express different learning strategies as birds from the different selection lines were differently affected by their previous learning performance.
    https://doi.org/10.1007/s10071-012-0500-3
  • General and Comparative Endocrinology
    2012

    Corticosterone responses differ between lines of great tits (Parus major) selected for divergent personalities

    A.T. Baugh, Sonja Schaper, M. Hau, J.F. Cockrem, Piet De Goede, Kees van Oers
    Animal ‘personality’ describes consistent individual differences in suites of behaviors, a phenomenon exhibited in diverse animal taxa and shown to be under natural and sexual selection. It has been suggested that variation in personality reflects underlying physiological variation; however there is limited empirical evidence to test this hypothesis in wild animals. The hypothalamic–pituitary–adrenal axis is hypothesized to play a central role in personality variation. Here we tested whether in great tits Parus major variation in personality traits is related to plasma concentrations of corticosterone (CORT). Using a capture-restraint protocol we examined baseline and stress-induced CORT levels in two captive experimental groups: (1) birds selected for divergent personalities (‘fast-bold’ and ‘slow-shy’ explorers); and (2) non-selected offspring of wild parents. We first tested for differences in CORT between selection lines, and second examined the relationship between responses in a canonical personality test and CORT concentrations in non-selected birds. We found support for our prediction that the slow-shy line would exhibit a higher acute stress response than the fast-bold line, indicating a genetic correlation between exploratory behavior and stress physiology. We did not, however, find that continuous variation in exploratory behavior co-varies with CORT concentrations in non-selected birds. While our results provide support for the idea that personality emerges as a result of correlated selection on behavior and underlying physiological mechanisms, they also indicate that this link may be particularly evident when composite personality traits are the target of selection.
    https://doi.org/10.1016/j.ygcen.2011.12.012
  • Animal Behaviour
    2012

    Personality affects learning performance in difficult tasks in a sex-dependent way

    Mieke Titulaer, Kees van Oers, Marc Naguib
    Animals constantly need to cope with changes in their environment. Coping with changes in cues that are associated with the location and abundance of food is essential for being able to adjust behaviourally to a variable environment. The use of cues in decision making requires appropriate levels of attention and learning ability, which may be affected by the personality of an individual. The relationship between personality, attention and learning as essential mechanisms for behavioural adaptation, however, is not well understood. We studied the relationship between attention to environmental cues, behavioural flexibility in learning and exploratory behaviour, a proxy for personality, in great tits, Parus major. We used a dimensional shift learning paradigm; a learning task involving several stages differing in complexity and requiring attention to changes in relevant cues. The results show personality differences in performance in learning flexibility in only the apparently most difficult stage, yet in opposite directions for males and females. Fast-exploring males showed more flexible learning abilities than slow males, whereas in females slow explorers outperformed fast explorers. These context-dependent and sex-specific personality effects reveal behavioural and cognitive mechanisms that may underlie observed sex- and personality-dependent fitness differences in natural populations.
    https://doi.org/10.1016/j.anbehav.2011.12.020
  • Ethology
    2012

    Song amplitude of rival males modulates the territorial behaviour of great tits during the fertile period of their mates

    M. Ritschard, Kees van Oers, Marc Naguib, H. Brumm
    Bird song is a widely used model in the study of sexual selection. Variation in the expression of sexually selected traits is thought to reflect variation in male genetic and/or phenotypic quality. Vocal amplitude is a song parameter that has received little attention in the context of sexual selection, but there is some evidence that the intensity of bird song affects female preferences. Here, we tested whether the amplitude of broadcast song plays a role in male–male competition. We used song playback with varying song amplitude (within the natural amplitude range of the species) and a dummy bird taxidermy to simulate territorial intrusions in the great tit, Parus major, during the fertile period of the female and measured the response of the local male. The results show that playback amplitude significantly affected the subjects’ behaviour: after approaching to within 25 m around the loudspeaker, territorial males stayed longer within that perimeter after the playback of high-amplitude songs compared with low-amplitude songs. Our findings add to the small but growing body of evidence suggesting that vocal amplitude may be a sexually selected song trait.
    https://doi.org/10.1111/j.1439-0310.2011.01999.x
  • Behavioral Ecology
    2012

    Boldness affects foraging decisions in barnacle geese: an experimental approach

    R.H.J.M. Kurvers, Bart A. Nolet, H.H.T. Prins, R.C. Ydenburg, Kees van Oers
    Individuals foraging in groups constantly need to make decisions, such as when to leave a group, when to join a group, and when to move collectively to another feeding site. In recent years, it has become evident that personality may affect these foraging decisions, but studies where individuals are experimentally forced into different roles are still absent. Here, we forced individual barnacle geese, Branta leucopsis, differing in boldness scores, either in a joining or in a leaving role in a feeding context. We placed a food patch at the far end of a test arena and measured the arrival latency and number of visits of individuals to the patch either in the presence of a companion that was confined near the food patch (“joining context”) or in the presence of a companion that was confined away from the food patch (“leaving context”). We also ran trials without a companion (“nonsocial context”). Bolder individuals arrived more quickly than shyer individuals in the “leaving” context, but there was no effect of boldness in the “joining” context, suggesting that boldness differences are important in explaining variation in leaving behavior but not in joining behavior. The difference in arrival latency between the “joining” and non-social context increased with decreasing boldness score, suggesting that shyer individuals are more responsive to the presence of other individuals (i.e., social facilitation). These results indicate that individual differences in boldness play a role in patch choice decisions of group-living animals, such as when to leave a flock and when to join others at a patch.
    https://doi.org/10.1093/beheco/ars091
  • Ardea
    2012

    Volume of the cloacal protuberance as an indication of reproductive state in male Blue Tits Cyanistes caeruleus.

    E. Schut, M.J.L. Magrath, Kees van Oers, J. Komdeur
    In male passerines, the accumulation of sperm in the sperm reserves causes the cloaca to become enlarged, forming the cloacal protuberance (CP). In Blue Tits, the timing of breeding differs considerably between pairs. Hence, when catching a male during the breeding season it may be unclear whether he is in a reproductively active state (i.e. producing sperm). Here, we show in captive Blue Tits Cyanistes caeruleus that CP volume is increased in males in a reproductively active state when compared to the same males in a reproductively inactive state. However, there was some overlap in CP volume when comparing the values in reproductively active and non-active states. Measurements of CP volume at a single time point, therefore, do not allow the researcher to reliably determine an individual’s reproductive status.
    https://doi.org/10.5253/078.100.0212
  • Developmental Psychobiology
    2011

    Effects of social conditions during early development on stress response and personality traits in great tits (Parus major)

    Marc Naguib, C. Flörcke, Kees van Oers
    Environmental conditions during early development play a crucial role in shaping an organism's phenotype. To test how social group size affects stress response and behavioral characteristics, we used great tits (Parus major) from selection lines for exploratory behavior, a proxy for an avian personality trait, and birds from the wild in a brood size manipulation experiment. Nestlings were tested for stress response using an established stress test and after independence subjects were tested for exploratory behavior. Nestlings from small broods showed a stronger stress response than nestlings from normal-sized broods. Exploratory behavior was not affected by brood size but associated with sex ratio in the nest. Birds from female-biased broods became faster explorers than those from male-biased broods. The results demonstrate that early social conditions can affect physiological stress responses in nestlings and that behavioral personality traits measured after fledging can be affected by the social experience in the nest.
    https://doi.org/10.1002/dev.20533
  • Animal Behaviour
    2011

    Correlated response to selection of testosterone levels and immunocompetence in lines selected for avian personality

    Kees van Oers, K.L. Buchanan, T.E. Thomas, P.J. Drent
    Individuals within species differ in their behavioural reactions to the environment. Consistent individual differences in these behaviours (personality traits) are often correlated and known to be under natural selection. These differences are frequently associated with variation in physiological traits, such as endocrine profiles. For example, variation in circulating testosterone levels is associated with variation in several personality traits and has been hypothesized to be a marker for personality in humans and rodents. The importance of testosterone in controlling both behavioural strategies and individual physiological differences suggests that direct selection on personality traits might cause pleiotropic selection on the physiological mechanisms underlying these traits. To test this hypothesis, we quantified levels of plasma testosterone levels and measured phytohaemagglutinin (PHA)-induced immune responses of male great tits, Parus major, in lines artificially selected for diverging levels of avian personality (‘fast’ and ‘slow’ exploratory behaviour). We found that testosterone levels were highly repeatable within individuals and fluctuated predictably over the season. Contrary to our expectations, ‘slow’ explorers had consistently higher levels of baseline testosterone and higher immune responses than ‘fast’ explorers. These results show that phenotypic selection for variation in personality traits corresponds to consistent differences in hormone profile and immune function, but that higher aggression levels do not need to be associated with higher baseline testosterone levels. Our results confirm that personality traits have evolved as a result of selection on both the underlying controlling physiological mechanisms and the phenotypic traits.
    https://doi.org/10.1016/j.anbehav.2011.02.014
  • 2011

    Towards a basis for the phenotypic gambit: advances in the evolutionary genetics of animal personality

    Kees van Oers, D.L. Sinn
    Individuals of many species, including humans, differ consistently in the way they behave. These consistent behavioral differences among individuals are collectively known as animal personality (Gosling 2001), behavioral syndromes (Sih et al. 2004a), behavioral strategies (Benus et al. 1990), or behavioral profiles (Rodgers et al. 1997). Each of these terms, to some extent, describe an emergent phenomenon of the total biases in behavioral reactions an individual expresses compared to other individuals within the same population or species. In other words, animal personality, in addition to referring to consistent differences between individuals, also refers to correlated behaviors. These correlations (usually defined at the level of populations of individuals) can occur through time (an individual that is bold at one time is also bold at another), across different functional contexts (an individual that is bold toward a predator is also aggressive toward conspecifics), or some combination of time and context (juvenile exploratory behavior is related to adult sociability). Although there is some debate on terminology (e.g., Réale et al. 2007; Gosling 2008), we use the term “animal personality” throughout this chapter.
    https://doi.org/10.1007/978-4-431-53892-9_7
  • 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
  • Journal of Ornithology
    2010

    Reduced blood parasite prevalence with age in the Seychelles Warbler: selecive mortality or suppression of infection?

    Kees van Oers, D. Richardson, S.A. Saether, J. Komdeur
    Avian malaria can affect survival and reproduction of their hosts. Two patterns commonly observed in birds are that females have a higher prevalence of malaria than do males and that prevalence decreases with age. The mechanisms behind these patterns remain unclear. However, most studies on blood parasite infections are based on cross-sectional analyses of prevalence, ignoring malaria related mortality and individual changes in infection. Here, we analyse both within-individual changes in malaria prevalence and long-term survival consequences of infection in the Seychelles Warbler (Acrocephalus sechellensis). Adults were less likely to be infected than juveniles but, contrary to broad patterns previously reported in birds, females were less likely to be infected than males. We show by screening individual birds in two subsequent years that the decline with age is a result both of individual suppression of infection and selective mortality. Birds that were infected early in life had a lower survival rate compared to uninfected birds, but among those that survived to be screened twice the proportion of infected birds had also decreased. Uninfected birds did not become infected later in life. Males were found to be more infected than females in this species possibly because, unlike most birds, males are the dispersing sex and the cost of dispersal may have to be traded against immunity. Infected males took longer to suppress their infection than did females. We conclude that these infections are indeed costly, and that age-related patterns in blood parasite prevalence are influenced both by suppression and selective mortality.
    https://doi.org/10.1007/s10336-009-0427-x
  • Ardea
    2010

    Black Terns Chlidonias niger and their dietary problems in Dutch wetlands

    A. Beintema, T. Baarspul, J.P. Krijger, Kees van Oers, Marek Keller
    Black Terns Chlidonias niger have shown a decrease of well over 90% as a breeding bird in The Netherlands during the twentieth century. Two hypotheses have been put forward for this decline: the disappearance of the floating plant Water Soldier Stratiotes aloides, which used to be the favourite nesting substrate of the terns, and a decrease of available insect food for the chicks, notably dragonflies. Both effects are attributed to eutrophication of surface waters. Reproductive bottlenecks vary greatly among areas and habitats. In river landscapes, no signs of food shortage could be found, and loss of nesting substrate has been successfully compensated for by offering artificial nest rafts. Extremely low fledging success in moors and in lowland grasslands is caused by food problems. In this case, artificial rafts are less successful. With decreased insect availability, fish and earthworms have become more important in the chicks' diet, but these are less reliable as a food source. Fledging success greatly depends on the amount of fish in the diet. Also, a minimum amount of fish is always needed to cover the calcium need of the chicks. In north-eastern Poland, there were no problems with either nesting places or food for the chicks.
    https://doi.org/10.5253/078.098.0310
  • 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, B.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
  • American Naturalist
    2010

    Passerine extrapair mating dynamics: a bayesian modeling approach comparing four species

    J.E. Brommer, J.S. Alho, C. Biard, J.R. Chapman, A. Charmantier, A. Dreiss, I.R. Hartley, M.B. Hjernquist, B. Kempenaers, J. Komdeur, T. Laaksonen, P.K. Lehtonen, T. Lubjuhn, S.C. Patrick, B. Rosivall, J.M. Tinbergen, M. Van der Velde, Kees van Oers, T. Wilk, W. Winkel
    In many socially monogamous animals, females engage in extrapair copulation (EPC), causing some broods to contain both within‐pair and extrapair young (EPY). The proportion of all young that are EPY varies across populations and species. Because an EPC that does not result in EPY leaves no forensic trace, this variation in the proportion of EPY reflects both variation in the tendency to engage in EPC and variation in the extrapair fertilization (EPF) process across populations and species. We analyzed data on the distribution of EPY in broods of four passerines (blue tit, great tit, collared flycatcher, and pied flycatcher), with 18,564 genotyped nestlings from 2,346 broods in two to nine populations per species. Our Bayesian modeling approach estimated the underlying probability function of EPC (assumed to be a Poisson function) and conditional binomial EPF probability. We used an information theoretical approach to show that the expected distribution of EPC per female varies across populations but that EPF probabilities vary on the above‐species level (tits vs. flycatchers). Hence, for these four passerines, our model suggests that the probability of an EPC mainly is determined by ecological (population‐specific) conditions, whereas EPF probabilities reflect processes that are fixed above the species level.
    https://doi.org/10.1086/653660
  • Ecology Letters
    2010

    Personality predicts the use of social information

    R.H.J.M. Kurvers, Kees van Oers, Bart A. Nolet, R.M. Jonker, S.E. Van Wieren, H.H.T. Prins, R.C. Ydenberg
    The use of social information is known to affect various important aspects of an individual’s ecology, such as foraging, dispersal and space use and is generally assumed to be entirely flexible and context dependent. However, the potential link between personality differences and social information use has received little attention. In this study, we studied whether use of social information was related to personality, using barnacle geese, Branta leucopsis, where boldness is a personality trait known to be consistent over time. We found that the use of social information decreased with increasing boldness score of the individuals. Individuals had lower feeding times when they did not follow the social information and this effect was unrelated to boldness score. When manipulating social information, thereby making it incorrect, individuals irrespective of their boldness score, learned that it was incorrect and ignored it. Our results show that social information use depends on the personality type of an individual, which calls for incorporation of these personality-related differences in studies of spatial distribution of animals in which social information use plays a role.
    https://doi.org/10.1111/j.1461-0248.2010.01473.x
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    2010

    Evolutionary genomics of animal personality

    Kees van Oers, J.C. Mueller
    Research on animal personality can be approached from both a phenotypic and a genetic perspective. While using a phenotypic approach one can measure present selection on personality traits and their combinations. However, this approach cannot reconstruct the historical trajectory that was taken by evolution. Therefore, it is essential for our understanding of the causes and consequences of personality diversity to link phenotypic variation in personality traits with polymorphisms in genomic regions that code for this trait variation. Identifying genes or genome regions that underlie personality traits will open exciting possibilities to study natural selection at the molecular level, gene–gene and gene–environment interactions, pleiotropic effects and how gene expression shapes personality phenotypes. In this paper, we will discuss how genome information revealed by already established approaches and some more recent techniques such as high-throughput sequencing of genomic regions in a large number of individuals can be used to infer micro-evolutionary processes, historical selection and finally the maintenance of personality trait variation. We will do this by reviewing recent advances in molecular genetics of animal personality, but will also use advanced human personality studies as case studies of how molecular information may be used in animal personality research in the near future.
    https://doi.org/10.1098/rstb.2010.0178
  • Proceedings of the Royal Society B-Biological Sciences
    2010

    The effect of personality on social foraging: shy barnacle geese scrounge more

    R.H.J.M. Kurvers, H.H.T. Prins, S.E. Van Wieren, Kees van Oers, Bart A. Nolet, R.C. Ydenberg
    Animals foraging in groups can either search for food themselves (producing) or search for the food discoveries of other individuals (scrounging). Tactic use in producer–scrounger games is partly flexible but individuals tend to show consistency in tactic use under different conditions suggesting that personality might play a role in tactic use in producer–scrounger games. Here we studied the use of producing and scrounging tactics by bold and shy barnacle geese (Branta leucopsis), where boldness is a personality trait known to be repeatable over time in this species. We defined individuals as bold, shy or intermediate based on two novel object tests. We scored the frequency of finding food patches (the outcome of investing in producing) and joining patches (the outcome of investing in scrounging) by bold and shy individuals and their feeding time. Shy individuals had a higher frequency of joining than bold individuals, demonstrating for the first time that personality is associated with tactic use in a producer–scrounger game. Bold individuals tended to spend more time feeding than shy individuals. Our results highlight the importance of including individual behavioural variation in models of producer–scrounger games.
    https://doi.org/10.1098/rspb.2009.1474
  • 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
  • Molecular Ecology
    2010

    Association between DRD4 gene polymorphism and personality variation in great tits: a test across four wild populations

    P. Korsten, J.C. Mueller, C. Hermannstädter, K.M. Bouwman, N.J. Dingemanse, P.J. Drent, M. Liedvogel, E. Matthysen, Kees van Oers, T. van Overveld, S.C. Patrick, J.G. Quinn, Ben C. Sheldon, J.M. Tinbergen, B. Kempenaers
    Polymorphisms in the dopamine receptor D4 gene (DRD4) have been related to individual variation in novelty-seeking or exploratory behaviour in a variety of animals, including humans. Recently, the human DRD4 orthologue was sequenced in a wild bird, the great tit (Parus major) and a single nucleotide polymorphism in exon 3 of this gene (SNP830) was shown to be associated with variation in exploratory behaviour of lab-raised individuals originating from a single wild population. Here we test the generality of this finding in a large sample of free-living individuals from four European great tit populations, including the originally sampled population. We demonstrate that the association between SNP830 genotype and exploratory behaviour also exists in free-living birds from the original population. However, in the other three populations we found only limited evidence for an association: in two populations the association appeared absent; while in one there was a nonsignificant tendency. We could not confirm a previously demonstrated interaction with another DRD4 polymorphism, a 15 bp indel in the promoter region (ID15). As yet unknown differences in genetic or environmental background could explain why the same genetic polymorphism (SNP830) has a substantial effect on exploratory behaviour in one population, explaining 4.5–5.8% of the total variance—a large effect for a single gene influencing a complex behavioural trait—but not in three others. The confirmation of an association between SNP830 genotype and personality-related behaviour in a wild bird population warrants further research into potential fitness effects of the polymorphism, while also the population differences in the strength of the association deserve further investigation. Another important future challenge is the identification of additional loci influencing avian personality traits in the wild.
    https://doi.org/10.1111/j.1365-294X.2009.04518.x
  • Animal Behaviour
    2009

    Experimental nest site limitation affects reproductive strategies and parental investment in a hole-nesting passerine

    A. Jacot, M. Valcu, Kees van Oers, B. Kempenaers
    In resource defence mating systems, males monopolize a resource that is of primary importance for breeding females. For secondary cavity nesters, the availability of suitable nesting sites is important in determining the strength of intrasexual competition, whereby phenotypic and behavioural traits will be favoured that enable individuals to gain access to these sites. The traits that are important in male competition may additionally affect mate choice decisions and a female's investment in the current brood. In a field study on blue tits, Cyanistes caeruleus, we increased intrasexual competition by experimentally limiting nest sites in experimental plots and compared these plots to control plots. Birds breeding in experimental plots did not differ phenotypically from birds in control plots. However, females that bred in the nest site-limited plots fed their offspring at a higher rate than control females. This result indicates that increased competition for limited resources led to more investment in current reproduction, either because successful females were of higher intrinsic quality or because they adjusted their investment in relation to superior territory or male characteristics.
    https://doi.org/10.1016/j.anbehav.2009.01.012
  • Ethology
    2009

    Handling stress as a measurement of personality in great tit nestlings (Parus major)

    E. Fučiková, P.J. Drent, N. Smits, Kees van Oers
    Interest in personality is growing in a wide range of disciplines, but only in a few systems it is possible to assess the survival value of personality. Field studies looking at the relationship between personality and survival value early in life are greatly hampered by the fact that personality can at present only be assessed after individuals become independent from their parents. In passerines, for example, this is often after a period of intensive selection for the survival on fledglings. The main aim of this study is therefore to develop a method to measure personality before this period of selection. For this purpose, we developed the handling stress (HS) test. We measured HS in 14-d-old great tit nestlings by counting the number of breast movements (breath rate) in four subsequent 15-s bouts for 1 min; before and after they were socially isolated from their siblings for 15 min. To calculate the repeatability of HS, we repeated the test 6 mo later. To assess the relat! ionship between HS and exploratory behaviour, we correlated the outcome of both tests. We ran tests both on birds of lines selected for extreme personality and on wild birds from a natural population. We found that birds selected for fast exploration reacted more to HS compared with birds selected for slow exploration and that HS was repeatable in different life phases. We confirmed this by finding an increase in the HS with increasing exploratory scores in wild birds. These results show that we can use the HS test as a measurement of personality, making it a potential tool for studying the relationship between personality and survival value early in life.
    https://doi.org/10.1111/j.1439-0310.2009.01618.x
  • Animal Behaviour
    2009

    Personality differences explain leadership in barnacle geese

    R.H.J.M. Kurvers, B. Eijkelenkamp, Kees van Oers, Bart van Lith, S.E. Van Wieren, R.C. Ydenberg, H.H.T. Prins
    Personality in animal behaviour describes the observation that behavioural differences between individuals are consistent over time and context. Studies of group-living animals show that movement order among individuals is also consistent over time and context, suggesting that some individuals lead and others follow. However, the relationship between leadership and personality traits is poorly studied. We measured several personality traits and leadership of individual barnacle geese, Branta leucopsis. We measured body size and scored the dominance of individuals living in a stable group situation before subjecting them to an open-field test, an activity test, a novel-object test, and a leadership test in which the order of the movement of individuals in pairs towards a feeding patch was scored. We found high repeatability for activity and novel-object scores over time. Leadership was strongly correlated with novel-object score but not with dominance rank, activity or exploration in an open field. These results provide evidence that leadership is closely related to some aspects of personality. Interestingly, an individual's arrival at the food patch was affected not only by the novel-object score of the focal individual, but also by the novel-object score of the companion individual, indicating that movement patterns of individuals living in groups are affected by the personality traits of other group members and suggesting that movement patterns of a group may be shaped by the mix of personality types present in the group.
    https://doi.org/10.1016/j.anbehav.2009.06.002
  • Animal Behaviour
    2008

    Personality is associated with extrapair paternity in great tits, Parus major

    Kees van Oers, P.J. Drent, N.J. Dingemanse, B. Kempenaers
    Animals differ in their behaviour comparable to how humans differ in personality: individuals consistently differ in suites of correlated traits. Relationships between ‘personality traits’ and fitness imply that personality traits can evolve by means of natural selection. We studied whether animal personality is also involved in sexual selection. We investigated whether exploratory behaviour (an aspect of animal personality, ranging from ‘slow’ to ‘fast’) correlated with the occurrence of extrapair paternity (EPP) in broods of wild great tits. We expected that EPP rates should be highest for females mated with social partners of the same personality type (i.e. for slow–slow or fast–fast pairs, but not other pair combinations). We found that the likelihood of EPP was highest for these pairs. Disassortative extrapair mating with respect to personality can be the consequence of several non-mutually exclusive processes. It might be caused by adaptive mate choice, which allows assortatively paired females to produce offspring with either more variable or more intermediate phenotypes, but it could also be the consequence of behavioural incompatibility between extreme behavioural phenotypes. Our findings indicate that personality differences play a role in the mechanism behind extrapair behaviours and we therefore conclude that it is now plausible that partner preference is based not only on morphological characteristics, but also on consistent behavioural traits or personality.
    https://doi.org/10.1016/j.anbehav.2008.03.011
  • European Journal of Personality
    2008

    Animal personality, behaviour or traits: What are we measuring?

    With the development of a new bottom-up methodology, the author aims at providing its with a tool for comparative personality research. This tool will indeed help us to identify differences between related species. However, to understand how differences within species are maintained and differences between species have evolved, we need to identify selection pressures on personality traits empirically
  • Journal of Ornithology
    2007

    Long-term effects of repeated handling and bleeding in wild caught Great Tits Parus major

    Kees van Oers, C. Carere
    Handling and bleeding are frequently used procedures in avian research and several studies show that they can exert short-term effects, such as elevation in corticosterone levels. However, the long-term effects of exposure to such manipulations are largely unknown, but could have important implications, especially for much of the long-term research on birds and experiments that involve longitudinal assessments. In this study, we evaluated the effect of handling and bleeding on some physiological and behavioural parameters. Hand-reared Great Tits Parus major originating from wild nests were used in two different experiments for other purposes. In these experiments, the birds were exposed to different frequencies of bleeding and handling events across a period of 45 days. The “high stress” group experienced a total of seven times handling and five times bleeding, while a “low stress” group was handled three times and bled only once. Thirty days after the experiments, when caught and handled from a cage, individuals of the high stress group were easier to catch, displayed significantly higher breath rates, and were more docile than individuals of the low stress group. No differences in body mass were detected. These results indicate that repeated manipulations cause evident long-term changes in coping with such procedures, which are likely due to learning effects, and provide empirical evidence that the past experimental history of an animal has to be taken into account in subsequent experiments.
    https://doi.org/10.1007/s10336-007-0200-y
  • Proceedings of the Royal Society B-Biological Sciences
    2007

    Drd4 gene polymorphisms are associated with personality variation in a passerine bird

    A.E. Fidler, Kees van Oers, P.J. Drent, S. Kuhn, J.C. Mueller, B. Kempenaers
    Polymorphisms in several neurotransmitter-associated genes have been associated with variation in human personality traits. Among the more promising of such associations is that between the human dopamine receptor D4 gene (Drd4) variants and novelty-seeking behaviour. However, genetic epistasis, genotype–environment interactions and confounding environmental factors all act to obscure genotype–personality relationships. Such problems can be addressed by measuring personality under standardized conditions and by selection experiments, with both approaches only feasible with non-human animals. Looking for similar Drd4 genotype–personality associations in a free-living bird, the great tit (Parus major), we detected 73 polymorphisms (66 SNPs, 7 indels) in the P. major Drd4 orthologue. Two of the P. major Drd4 gene polymorphisms were investigated for evidence of association with novelty-seeking behaviour: a coding region synonymous single nucleotide polymorphism (SNP830) and a 15bp indel (ID15) located 5′ to the putative transcription initiation site. Frequencies of the three Drd4 SNP830 genotypes, but not the ID15 genotypes, differed significantly between two P. major lines selected over four generations for divergent levels of ‘early exploratory behaviour’ (EEB). Strong corroborating evidence for the significance of this finding comes from the analysis of free-living, unselected birds where we found a significant association between SNP830 genotypes and differing mean EEB levels. These findings suggest that an association between Drd4 gene polymorphisms and animal personality variation predates the divergence of the avian and mammalian lineages. Furthermore, this work heralds the possibility of following microevolutionary changes in frequencies of behaviourally relevant Drd4 polymorphisms within populations where natural selection acts differentially on different personality types.
    https://doi.org/10.1098/rspb.2007.0337
  • European Journal of Personality
    2007

    The need for interdisciplinary research in personality studies

    The target paper demonstrates the value of evolutionary genetics for personality research. Apart from a summing-up of concepts, the authors validate their theory with evidence from studies on both human- and animal personality. In this commentary, I want to show the need for inter-disciplinary research to answer questions on personality in psychology and biology.
    https://doi.org/10.1002/per.646
  • Behavioral Ecology
    2005

    Context dependence of personalities: risk-taking behavior in a social and a nonsocial situation

    Kees van Oers, M. Klunder, P.J. Drent
    Individuals of many species differ consistently in their behavioral reaction to mild novel challenges. Suites of these behaviors are referred to as behavioral syndromes or personalities. Personality traits are often phenotypically and genetically correlated. Therefore, animal personalities are generally considered as broad characteristics, with one underlying genetical and physiological mechanism that is expressed across situations and contexts. Because there are carryover effects between situations, animals are not entirely flexible in their behavior in each situation. This may cause behaviors to seem nonadaptive in isolated situations. To test whether individuals with different personalities could react differently to changes in their environment, we studied context dependence of personalities in the great tit (Parus major). We tested birds categorized as either fast or slow explorers for their latency to come back to a feeding table after a mild startle (risk-taking behavior) in a nonsocial followed by a social context. We found that the relation between exploratory behavior and risk-taking behavior depended on the social context. Females in general returned later in the social test, while male reaction to the presence of a conspecific was dependent on their behavioral type. Slow males thereby reacted to the behavior of the companion and fast males did not. These results show that although personalities have a rigid structure the relation between personality traits is context dependent. These results are discussed in the perspective of the adaptive significance and maintenance of personalities. [KEYWORDS: Behavioral syndromes ; boldness ; exploration ; Parus major ; personality ; risk taking]
    https://doi.org/10.1093/beheco/ari045
  • Behaviour
    2005

    Contribution of genetics to the study of animal personalities: a review of case studies

    Kees van Oers, G. De Jong, Arie Van Noordwijk, B. Kempenaers, P.J. Drent
    The need for evolutionary studies on quantitative traits that integrate genetics is increasing. Studies on consistent individual differences in behavioural traits provide a good opportunity to do controlled experiments on the genetic mechanisms underlying the variation and covariation in complex behavioural traits. In this review we will highlight the contribution of genetic studies in animal personality research. We will start with reviewing the evidence that shows how much variation in animal personality traits is genetic, and connect this to knowledge from human personality studies. We will continue by considering the nature of that variation, its generation and maintenance. Finally we will point to further possibilities for studying the genetics of animal personalities. We will underline the importance of integrating both proximate and ultimate approaches when studying the evolution of animal personalities
    https://doi.org/10.1163/156853905774539364
  • Heredity
    2004

    Additive and nonadditive genetic variation in avian personality traits

    Kees van Oers, P.J. Drent, G. De Jong, Arie Van Noordwijk
    Individuals of all vertebrate species differ consistently in their reactions to mildly stressful challenges. These typical reactions, described as personalities or coping strategies, have a clear genetic basis, but the structure of their inheritance in natural populations is almost unknown. We carried out a quantitative genetic analysis of two personality traits (exploration and boldness) and the combination of these two traits (early exploratory behaviour). This study was carried out on the lines resulting from a two-directional artificial selection experiment on early exploratory behaviour (EEB) of great tits (Parus major) originating from a wild population. In analyses using the original lines, reciprocal F1 and reciprocal first backcross generations, additive, dominance, maternal effects ands sex-dependent expression of exploration, boldness and EEB were estimated. Both additive and dominant genetic effects were important determinants of phenotypic variation in exploratory behaviour and boldness. However, no sex-dependent expression was observed in either of these personality traits. These results are discussed with respect to the maintenance of genetic variation in personality traits, and the expected genetic structure of other behavioural and life history traits in general. [KEYWORDS: Parus major; personalities; exploration; boldness; sex-dependent expression; maternal effects]
    https://doi.org/10.1038/sj.hdy.6800530
  • Proceedings of the Royal Society B-Biological Sciences
    2004

    Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities

    Kees van Oers, P.J. Drent, Piet De Goede, Arie Van Noordwijk
    Personalities are general properties of humans and other animals. Different personality traits are phenotypically correlated, and heritabilities of personality traits have been reported in humans and various animals. In great tits, consistent heritable differences have been found in relation to exploration, which is correlated with various other personality traits. In this paper, we investigate whether or not risk-taking behaviour is part of these avian personalities. We found that (i) risk-taking behaviour is repeatable and correlated with exploratory behaviour in wild-caught hand-reared birds, (ii) in a bi-directional selection experiment on 'fast' and 'slow' early exploratory behaviour, bird lines tend to differ in risk-taking behaviour, and (iii) within-nest variation of risk-taking behaviour is smaller than between-nest variation. To show that risk-taking behaviour has a genetic component in a natural bird population, we bred great tits in the laboratory and artificially selected 'high' and 'low' risk-taking behaviour for two generations. Here, we report a realized heritability of 19.3 - 3.3% (s.e.m.) for risk-taking behaviour. With these results we show in several ways that risk-taking behaviour is linked to exploratory behaviour, and we therefore have evidence for the existence of avian personalities. Moreover, we prove that there is heritable variation in more than one correlated personality trait in a natural population, which demonstrates the potential for correlated evolution. [KEYWORDS: selection response; risk-taking behaviour; Parus major; approach-avoidance; temperament; personality]
    https://doi.org/10.1098/rspb.2003.2518
  • Behavior Genetics
    2004

    A genetic analysis of avian personality traits: correlated, response to artificial selection

    Kees van Oers, G. De Jong, P.J. Drent, Arie Van Noordwijk
    Individuals in a range of species consistently differ in their behavior towards mild challenges, over age and time. Differences have been found for several personality traits in a range of species. In great tits these traits have a genetic basis and are phenotypically correlated. Estimates of genetic correlations are, however, fundamental to understanding the evolution of consistent individual differences in behavior. This study analyzed two selection experiments on two avian personality traits, early exploratory behavior and risk-taking behavior. The selection lines used were both started using wild great tits (Parus major) from two natural populations. Genetic correlations were calculated using the response and the correlated response to artificial selection. We found genetic correlations ranging from 0.51 to 0.66, based on individual values, and from 0.84 to 1.00 based on nest means. Genetic correlations can be due to pleiotropic effects or to linkage disequilibrium. The different behavioral traits might therefore have a common genetic basis, possibly constraining independent evolution of personality traits in natural populations. These results are discussed in relation to domain generality and domain specificity of personalities. [KEYWORDS: boldness; exploration; genetic correlation; Parus major; personalities; risk-taking behavior]
    https://doi.org/10.1007/s10519-004-5588-z
  • 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
  • Physiology & Behavior
    2004

    Shy and bold great tits (Parus major): body temperature and breath rate in response to handling stress

    C. Carere, Kees van Oers
    A standard handling protocol was used to test the hypothesis that boldness predicts stress responsiveness in body temperature and breath rate. Great tit (Parus major) nestlings were taken from the field, hand reared until independence, and their response to a novel object was assessed. At the age of 6 months, during the active phase (daytime), body temperature was recorded and breath rate was counted immediately after capture and after 5 min of quiet rest in a bag. A second group of birds of two lines bidirectionally selected for the same trait was tested during the inactive phase (nighttime). During the active phase, body temperature and breath rate were higher in the first than in the second measurement. In the second measurement, shy individuals showed higher body temperature than bold individuals. In the inactive phase, values of both parameters were lower than in the active phase. Body temperature was lower in the first measurement than in the second measurement and no line difference emerged. Breath rate was higher in shy than in bold individuals and did not differ between the two measurements. Females had higher body temperatures than males, probably due to their lower weight, because body temperature was negatively correlated with body mass. The results indicate that body temperature and breath rate are indicators of acute stress in songbirds and that differences in personality traits during the juvenile phase are reflected in differential stress responsiveness later in life. [KEYWORDS: Handling stress ; Coping; Boldness ; Personality; Breath rate ; Body temperature ; Sex differences ; Birds]
    https://doi.org/10.1016/j.physbeh.2004.07.009
  • Proceedings of the Royal Society B-Biological Sciences
    2003

    Realized heritability of personalities in the great tit (Parus major)

    P.J. Drent, Kees van Oers, Arie Van Noordwijk
    Behaviour under conditions of mild stress shows consistent patterns in all vertebrates: exploratory behaviour, boldness, aggressiveness covary in the same way. The existence of highly consistent individual variation in these behavioural strategies, also referred to as personalities or coping styles, allows us to measure the behaviour under standardized conditions on birds bred in captivity, link the standardized measurements to the behaviour under natural conditions and measure natural selection in the field. We have bred the great tit (Parus major), a classical model species for the study of behaviour under natural conditions, in captivity. Here, we report a realized heritability of 54 ± 5% for early exploratory behaviour, based on four generations of bi-directional artificial selection. In addition to this, we measured hand-reared juveniles and their wild-caught parents in the laboratory. The heritability found in the mid-offspring-mid-parent regression was significantly different from zero. We have thus established the presence of considerable amounts of genetic variation for personality types in a wild bird.
    https://doi.org/10.1098/rspb.2002.2168
  • Ibis
    2002

    Anthelmintic treatment negatively affects chick survival in the Eurasian Oystercatcher Haematopus ostralegus

    Kees van Oers, D. Heg, S. Le Drean Quenec'du
    Eurasian Oystercatchers Haematopus ostralegus are infested with a wide range of gut parasites, but experimental evidence of their effects on host fitness is scant. We investigated prevalence of parasites, and experimentally tested the effects of gut parasites on chick survival and growth. One hundred and fifty-nine hatchlings from 66 nests were treated with a single dose anthelminthic medicine (0.5 mL Spectril + 0.0025 mL Ivomec) and compared with a sham-treated control group of 163 hatchlings from 66 nests. Unexpectedly, chicks treated with the anthelminthic drug survived less well than control chicks. Fledglings from the treated group were significantly less infected with gut parasites than untreated fledglings, although they were of similar body mass. One possible explanation for these findings is that the treatment interferes with the development of the immune system in the hatchlings. This might have caused mass mortality of treated hatchlings after the drug ceased to work and the treated chicks became susceptible to infections for the first time. Furthermore, all chicks and adults from both saltmarsh and adjacent freshwater habitat appeared free from blood parasites. Thus, in the Eurasian Oystercatcher, we found no support for the hypothesis, based on between-species comparisons, that the presence of blood parasites is related to the saltiness of the environment.
    https://doi.org/10.1046/j.1474-919X.2002.00078.x
  • Animal Behaviour
    2002

    Repeatability and heritability of exploratory behaviour in great tits from the wild

    N.J. Dingemanse, Christiaan Both, P.J. Drent, Kees van Oers, Arie Van Noordwijk
    We investigated whether individual great tits, Parus major, vary consistently in their exploratory behaviour in a novel environment and measured the repeatability and heritability of this trait. Wild birds were caught in their natural habitat, tested in the laboratory in an open field test on the following morning, then released at the capture site. We measured individual consistency of exploratory behaviour for recaptured individuals (repeatability) and estimated the heritability with parent–offspring regressions and sibling analyses. Measures of exploratory behaviour of individuals at repeated captures were consistent in both sexes and study areas (repeatabilities ranged from 0.27 to 0.48). Exploration scores did not differ between the sexes, and were unrelated to age, condition at fledging or condition during measurement. Heritability estimates were 0.22–0.41 (parent–offspring regressions) and 0.37–0.40 (sibling analyses). We conclude that (1) consistent individual variation in open field behaviour exists in individuals from the wild, and (2) this behavioural variation is heritable. This is one of the first studies showing heritable variation in a behavioural trait in animals from the wild, and poses the question of how this variation is maintained under natural conditions.
    https://doi.org/10.1006/anbe.2002.2006

Projects & collaborations

Projects

  • What makes innovative animals innovative?

    Project 2020–2023
    Innovation ability allows animals to invent plastic behavioural responses to various novel ecological challenges, thereby making it possible to exploit new resources. Until now, studies have generally focused on innovation ability as a factor on its own and very little is known about how various cognitive and behavioural traits co-operate in their effect on innovation ability. These traits may be cognitive and behavioural specializations, meaning they have evolved for specific functions other than innovation, but act together to allow animals to innovate. The behavioural and cognitive traits that may affect innovation ability will vary between species and between populations of the same species living in different environments. My main purpose in this project is to try, by as many means as possible, to pinpoint core differences between innovators and non-innovators. I aim to do this by making both inter- and intraspecific comparisons of performance in cognitive and behavioural essays in three species from Paridae family.
    koolmees
  • Ecological epigenetics and the brain: the evolutionary consequences of epigenomic modifications in a songbird

    Project 2018–2022
    This unique inter-disciplinary collaboration between three of the larger institutes of the KNAW aims to elucidate the function of epigenetic regulation in the...
    A multi-institute collaborative project
  • Epigenetics of animal personality: DNA methylation and its influence on exploratory behaviour in great tits

    Project 2018–2022
    Recent studies have shown that early developmental effects and environmental conditions experienced by parents also affect personality traits, even over multiple generations. Yet, the mechanisms underlying such transgenerational regulation remain unknown, while determining them is crucial to understand how development affects heritable traits in evolutionary processes.
    Koolmees_snow_
  • Predicting the evolution of an avian trait under human-induced natural selection

    Project 2018–2021
    This project aims to predict the genetic and the phenotypic changes of a trait that is expected to be under directional selection: beak size in great tits.
    gans

Outreach

Categories