Droevendaalsesteeg 10
6708 PB Wageningen
The Netherlands
Christa Mateman
Over
As a technician for the Animal Ecology department I am involved in the molecular analysis of samples. We use a relational database for collection management which makes it possible to compare phenotype with genotypes.
Biografie
Ing. Christa Mateman (1970) graduated as biochemical technician in 1993 at the "Hogeschool Enschede". In her final year she worked as a student at the NIZO (Netherlands Institute for Dairy Research) developing markers for detection and identification of lactic acid bacteria. She started working for the NIOO in 1993, initially for the Department of Plant Population Biology and subsequently for the Department of Animal Ecology. Her work involves developing techniques for sexing birds, screening for extra pair copulation's (microsatellites), studying genetic variation (next generation sequencing, SNP-detection) and gene expression (qPCR). She is also involved in the management of the samples collected within the department.
Onderzoeksgroepen
CV
Publicaties
Peer-reviewed publicaties
Developmental stress does not induce genome‐wide DNA methylation changes in wild great tit (Parus major) nestlings
The environment experienced during early life is a crucial factor in the life of many organisms. This early life environment has been shown to have profound effects on morphology, physiology and fitness. However, the molecular mechanisms that mediate these effects are largely unknown, even though they are essential for our understanding of the processes that induce phenotypic variation in natural populations. DNA methylation is an epigenetic mechanism that has been suggested to explain such environmentally induced phenotypic changes early in life. To investigate whether DNA methylation changes are associated with experimentally induced early developmental effects, we cross-fostered great tit (Parus major) nestlings and manipulated their brood sizes in a natural study population. We assessed experimental brood size effects on pre-fledging biometry and behaviour. We linked this to genome-wide DNA methylation levels of CpG sites in erythrocyte DNA, using 122 individuals and an improved epiGBS2 laboratory protocol. Brood enlargement caused developmental stress and negatively affected nestling condition, predominantly during the second half of the breeding season, when conditions are harsher. Brood enlargement, however, affected nestling DNA methylation in only one CpG site and only if the hatch date was taken into account. In conclusion, this study shows that nutritional stress in enlarged broods does not associate with direct effects on genome-wide DNA methylation. Future studies should assess whether genome-wide DNA methylation variation may arise later in life as a consequence of phenotypic changes during early development.https://doi.org/10.1111/mec.16973Integrated molecular and behavioural data reveal deep circadian disruption in response to artificial light at night in male Great tits (Parus major)
https://doi.org/10.1038/s41598-022-05059-4Globally 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.
epiGBS2
https://doi.org/10.1111/1755-0998.13597Several 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).
Exploration of tissue-specific gene expression patterns underlying timing of breeding in contrasting temperature environments in a song bird
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/s12864-019-6043-0The Genomics of Circadian Timing in a Wild Bird, the Great Tit (Parus major)
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.2019.00152Fine-tuning of seasonal timing of breeding is regulated downstream in the underlying neuro-endocrine system in a small songbird
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.202481Genetic and phenotypic responses to genomic selection for timing of breeding in a wild songbird
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.https://doi.org/10.1111/1365-2435.13360
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.Effects of experimental light at night on extra-pair paternity in a songbird
Abstract Light pollution is increasing worldwide and significantly affects animal behavior. In birds, these effects include advancement of morning activity and onset of dawn song, which may affect extra-pair paternity. Advanced dawn song of males may stimulate females to engage in extra-pair copulations, and the earlier activity onset may affect the males? mate guarding behavior. Earlier work showed an effect of light at night on extra-pair behavior, but this was in an area with other anthropogenic disturbances. Here, we present a two-year experimental study on effects of light at night on extra-pair paternity of great tits (Parus major). Previously dark natural areas were illuminated with white, red, and green LED lamps and compared to a dark control. In 2014, the proportion of extra-pair young in broods increased with distance to the red and white lamps (i.e., at lower light intensities), but decreased with distance to the poles in the dark control. In 2013, we found no effects on the proportion of extra-pair young. The total number of offspring sired by a male was unaffected by artificial light at night in both years, suggesting that potential changes in female fidelity in pairs breeding close to white and red light did not translate into fitness benefits for the males of these pairs. Artificial light at night might disrupt the natural patterns of extra-pair paternity, possibly negates potential benefits of extra-pair copulations and thus could alter sexual selection processes in wild birds.https://doi.org/10.1002/jez.2193Early arrival is not associated with more extra-pair fertilizations in a long-distance migratory bird
When assessing the benefits of early arrival date of migratory birds, a hidden and often ignored component of males’ fitness is the higher chance of early-arriving birds to obtain extra-pair fertilizations. Here we investigated how extra-pair paternity might affect the relationship between male arrival date and number of fertilizations in a model study system, the European pied flycatcher Ficedula hypoleuca. For this purpose, we sampled and genotyped breeding pairs, unpaired males and offspring (including embryos from unhatched eggs when possible) of a Dutch pied flycatcher population. Detailed information on arrival date of males, egg laying date of their social mates and nest success was also recorded. Early-arriving males had early-laying females and males with early-laying females had a higher probability of siring extra-pair eggs and obtain more fertilizations. However, male arrival date alone did not correlate with the probability to gain extra-pair paternity and neither to the amount of fertilized eggs. Both early- and late-arriving males had a higher probability of losing paternity in their own nest compared to birds with an intermediate arrival date. Finally, late-arriving males were more likely to remain unpaired but, interestingly, a few of these birds obtained paternity via extra-pair copulations. Because earlier arrival date did not lead to more extra-pair fertilizations and because such relationship seems to be driven mainly by the female's laying date, we conclude that the contribution of extra-pair paternity to the overall fitness benefits of early male arrival date is relatively small.https://doi.org/10.1111/jav.01317Evidence from Pyrosequencing Indicates that Natural Variation in Animal Personality is Associated with DRD4 DNA Methylation
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.13519The genome of the winter moth (Operophtera brumata) provides a genomic perspective on sexual dimorphism and phenology
The winter moth (Operophtera brumata) belongs to one of the most species-rich families in Lepidoptera, the Geometridae (approx. 23,000 species). This family is of great economic importance as most species are herbivorous and capable of defoliating trees. Genome assembly of the winter moth allows the study of genes and gene families, such as the cytochrome P450 gene family, which is known to be vital in plant secondary metabolite detoxification and host plant selection. It also enables exploration of the genomic basis for female brachyptery (wing reduction), a feature of sexual dimorphism in winter moth, and for seasonal timing, a trait extensively studied in this species. Here we present a reference genome for the winter moth, the first geometrid and largest sequenced Lepidopteran genome to date (638 Mb) including a set of 16,912 predicted protein-coding genes. This allowed us to assess the dynamics of evolution on a genome wide scale using the P450 gene family. We also identified an expanded gene family potentially linked to female brachyptery, and annotated the genes involved in the circadian clock mechanism as main candidates for involvement in seasonal timing. The genome will contribute to Lepidopteran genomic resources and comparative genomics. In addition, the genome enhances our ability to understand the genetic and molecular basis of insect seasonal timing and thereby provides a reference for future evolutionary and population studies on the winter moth.https://doi.org/10.1093/gbe/evv145Costs of sleeping in: circadian rhythms influence cuckoldry risk in a songbird
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/10.1111/1365-2435.12440Transfer of maternal antibodies against avian influenza virus in mallards (Anas platyrhynchos)
Maternal antibodies protect chicks from infection with pathogens early in life and may impact pathogen dynamics due to the alteration of the proportion of susceptible individuals in a population. We investigated the transfer of maternal antibodies against avian influenza virus (AIV) in a key AIV host species, the mallard (Anas platyrhynchos). Combining observations in both the field and in mallards kept in captivity, we connected maternal AIV antibody concentrations in eggs to (i) female body condition, (ii) female AIV antibody concentration, (iii) egg laying order, (iv) egg size and (v) embryo sex. We applied maternity analysis to the eggs collected in the field to account for intraspecific nest parasitism, which is reportedly high in Anseriformes, detecting parasitic eggs in one out of eight clutches. AIV antibody prevalence in free-living and captive females was respectively 48% and 56%, with 43% and 24% of the eggs receiving these antibodies maternally. In both field and captive study, maternal AIV antibody concentrations in egg yolk correlated positively with circulating AIV antibody concentrations in females. In the captive study, yolk AIV antibody concentrations correlated positively with egg laying order. Female body mass and egg size from the field and captive study, and embryos sex from the field study were not associated with maternal AIV antibody concentrations in eggs. Our study indicates that maternal AIV antibody transfer may potentially play an important role in shaping AIV infection dynamics in mallards.https://doi.org/10.1371/journal.pone.0112595Opposite differential allocation by males and females of the same species
Differential allocation (DA)—the adjustment of an individual’s parental investment in relation to its mate’s attractiveness—is increasingly recognized as an important component of sexual selection. However, although DA is expected by both sexes of parents in species with biparental care, DA by males has rarely been investigated. We have previously demonstrated a decrease in the feeding rates of female blue tits Cyanistes caeruleus when their mate’s UV coloration was experimentally reduced (i.e. positive DA). In this study, we used the same experimental protocol in the same population to investigate DA by male blue tits in relation to their female’s UV coloration. Males mated to UV-reduced females had higher feeding rates than those mated to control females (i.e. negative DA). Thus, male and female blue tits display opposite DA for the same component of parental effort (chick provisioning), the first time that this has been reported for any species.https://doi.org/10.1098/rsbl.2012.0835Parental care and UV coloration in blue tits: opposite correlations in males and females between provisioning rate and mate’s coloration
Parental investment and sexually-selected signals can be intimately related, either because the signals indicate the amount of investment that an individual is prepared to make, and hence its value as a mate (the ‘good parent process’), or because individuals are selected to vary their own investment in relation to their mate’s signals (‘differential allocation’ or ‘reproductive compensation’). Correlations between parental investment and the sexually selected signals of both an individual and its mate are therefore of central interest in sexual selection. Blue tits Cyanistes caeruleus are an ideal study species to investigate such correlations because they provide substantial amounts of biparental care and possess sexually-selected structural UV coloration that seems to signal attractiveness in both sexes. We investigated whether feeding rates of male and female blue tits were correlated with either their own or their mate’s UV coloration, and whether any such correlation was affected by the sex ratio of the brood. We also investigated whether any such correlations were reflected in offspring phenotype. Feeding rates were not correlated with either sex of parent’s own UV coloration. However, they were correlated with the mate’s UV coloration, but in opposite directions in males and females: females had higher feeding rates when mated to bright UV males, implying differential allocation, while males had lower feeding rates when mated to bright UV females, implying reproductive compensation. These relationships were unaffected by the sex ratio of the brood. In addition, fledgling tarsus length, but not mass, was related to male UV coloration, and to female UV coloration in interaction with male age. These results suggest that both male and female attractiveness influence parental investment of the mate, and that this in turn affects offspring phenotype. We found no evidence for differential sex allocation.https://doi.org/10.1111/j.1600-048X.2012.05575.xThe design and cross-population application of a genome-wide SNP chip for the great tit Parus major
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.xAn additional field method to sex adult Barn Swallows during the non-breeding season in Zambia: white spot length in the outer tail feather
Adult Barn Swallows Hirundo rustica exhibit strong sexual size dimorphism in the length of the outermost tail feathers, which are longer in males compared with females. This trait is traditionally used to sex adult Barn Swallows in the field. However, due to the wear and breakage of the tips of the outer tail feather and tail moult during the non-breeding season, sexing becomes unreliable or even impossible. We therefore tested whether the length of the white spot on the outer tail feather is sexually dimorphic, and whether it can be used as an additional sexing method for adult Barn Swallows. The white spot length was sexually dimorphic, based on DNA analysis of 101 adult individuals caught at their roost during the non-breeding season in Zambia. Accuracy in sex determination of 95% could be obtained by classifying individuals with a white spot length 29.5 mm as males. When applying the length of the white spot as an additional method to sex adult Barn Swallows on all birds caught in Zambia during the study period (N = 759), the percentage of birds that could successfully be sexed increased to more than 55%. Therefore we emphasise the importance of measuring the white spot length in addition to the tail fork depth and tail length to sex adult Barn Swallows in the non-breeding season.https://doi.org/10.2989/00306525.2011.603467Neutral markers mirror small-scale quatitative genetic differentiation in an avian island population
We still know remarkably little about the extent to which neutral markers can provide a biologically relevant description of population structure. In the present study, we address this question, and quantify microsatellite differentiation among a small, structured island population of great tits (Parus major), and a large mainland population 150 km away. Although only a few kilometres apart, we found small but statistically significant levels of differentiation between the eastern and the western part of the island. On the other hand, there was no differentiation between the western part of the island and the mainland population, whereas the eastern part and the mainland did differ significantly. This initially counterintuitive result provides powerful support for the hypothesis that the large genetic difference in clutch size between both parts of the island found earlier is maintained by different levels of gene flow into both parts of the island, and illustrates the capac! ity of microsatellites to provide a meaningful description of population structure. Importantly, because the level of microsatellite differentiation is very low, we were unable to infer any population structure without grouping individuals a priori. Hence, these low levels of differentiation in neutral markers could easily remain undetected, or incorrectly be dismissed as biologically irrelevant. Thus, although microsatellites can provide a powerful tool to study genetic structure in wild populations, they should be used in conjunction with a range of other sources of information, rather than as a replacement.https://doi.org/10.1111/j.1095-8312.2009.01252.xPrimary sex ratio adjustment to experimentally reduced male UV attractiveness in blue tits
The study of primary sex ratio adjustment in birds is notorious for inconsistency of results among studies. To develop our understanding of avian sex ratio variation, experiments that test a priori predictions and the replication of previous studies are essential. We tested if female blue tits Parus caeruleus adjust the sex ratio of their offspring to the sexual attractiveness of their mates, as was suggested by a previous benchmark study on the same species. In 2 years, we reduced the ultraviolet (UV) reflectance of the crown feathers of males in the period before egg laying to decrease their attractiveness. In contrast to the simple prediction from sex allocation theory, we found that the overall proportion of male offspring did not differ between broods of UV-reduced and control-treated males. However, in 1 year, the UV treatment influenced offspring sex ratio depending on the natural crown UV reflectance of males before the treatment. The last result confirms the pattern found in the previous blue tit study, which suggests that these complex patterns of primary sex ratio variation are repeatable in this bird species, warranting further research into the adaptive value of blue tit sex ratio adjustment to male UV coloration. [KEYWORDS: blue tit Parus caeruleus, male attractiveness, primary sex ratio, sex allocation, ultraviolet plumage]https://doi.org/10.1093/beheco/arj061Consistent feeding positions of great tit parents
When parent birds arrive at the nest to provision their young, their position on the nest rim may influence which chick or chicks are fed. As a result, the consistency of feeding positions of the individual parents, and the difference in position between the parents, may affect how equitably food is divided among the chicks. We studied the positions of parent great tits, Parus major, landing on the nest to feed their chicks. Individual parents were consistent in their position within observation periods, on different days within the same breeding attempt, and at breeding attempts in different years. Within each sex, there were individual differences in position within single observation bouts, in average position across days within a breeding attempt, and in average position across years. At the majority of nests, the two parents differed in positions. The distribution of angular distances between the parents differed from that expected if the parents' positions were independent, with the observed median being less than that expected. The angular distance between the parents was not related to 22 different characteristics of the brood and parents. We conclude that consistency (i.e. a departure from a random uniform distribution) in position is explained by habit formation, and to a lesser extent by an overall preference for particular locations, and by nest configuration. We also conclude that there is little scope and no evidence for the parents strategically adjusting their angular separation.https://doi.org/10.1016/j.anbehav.2006.02.024Microsatellite loci in the European bee-eater, Merops apiaster
Twelve polymorphic microsatellite markers have been developed for the European bee-eater, Merops apiaster (Coraciiformes: Meropidae). Screening of eight individuals at these loci showed that the average allelic diversity was 5.8, with a range of two to 11 alleles per locus. The loci reported here will provide insight into the levels of extra-pair parentage, kin selection and dispersal in this species, which has co-operative breeding and nests in large colonies. [KEYWORDS: bee-eater Coraciiformes Meropidae Merops apiaster microsatellite]https://doi.org/10.1111/j.1471-8286.2004.00726.xFemale blue tits adjust parental effort to manipulated male UV attractiveness
The differential allocation hypothesis predicts that parents should adjust their current investment in relation to perceived mate attractiveness if this affects offspring fitness. It should be selectively advantageous to risk more of their future reproductive success by investing heavily in current offspring of high reproductive value but to decrease investment if offspring value is low. If the benefits of mate attractiveness are limited to a particular offspring sex we would instead expect relative investment in male versus female offspring to vary with mate attractiveness, referred to as 'differential sex allocation'. We present strong evidence for differential allocation of parental feeding effort in the wild and show an immediate effect on a component of offspring fitness. By experimentally reducing male UV crown coloration, a trait known to indicate attractiveness and viability in wild-breeding blue tits (Parus caeruleus), we show that females, but not males, reduce parental feeding rates and that this reduces the skeletal growth of offspring. However, differential sex allocation does not occur. We conclude that blue tit females use male UV coloration as an indicator of expected offspring fitness and adjust their investment accordingly. [KEYWORDS: differential allocation, differential sex allocation, parental effort, blue tit, UV coloration, mate attractiveness]https://doi.org/10.1098/rspb.2004.2825Sexual size dimorphism in the critically endangered Seychelles Scops Owl Otus insularis
The Seychelles Scops Owl Otus insularis is a critically endangered species restricted to the forests of Mahé in the Republic of Seychelles, Western Indian Ocean. This study presents the first biometric data collected from live individuals and investigates the occurence of sexual size dimorphism. Thirty-one birds were measured, and 30 of these were sexed by molecular analysis of their DNA: 6 females and 24 males. Females were generally heavier and larger than males. There was some variation in plumage colouration, which was unrelated to sex, but no evidence of distinct colour morphs as has been documented in other Western Indian Ocean Otus species.https://doi.org/10.1080/03078698.2002.9674272A molecular phylogeny of the dove genera Streptopelia and Columba
Evolutionary history of the dove genus Streptopelia has not been examined with rigorous phylogenetic methods. We present a study of phylogenetic relationships of Streptopelia based on over 3,600 base pairs of nuclear and mitochondrial gone sequences. To test for monophyly of Streptopelia, we used several other columbiform taxa, including Columba (Old and New World), Macropygia, Reinwardtoena, and the enigmatic Pink Pigeon (Nesoenas mayeri). On the basis of our analyses, Streptopelia (as currently defined) is not monophyletic; Nesoenas mayeri is the sister species to S. picturata, resulting in paraphyly of Streptopelia. Three main clades of Streptopelia are identified: (1) S. chinensis plus S. senegalensis, (2) S. picturata plus Nesoenas Mayeri, and (3) all other species of Streptopelia. It is unclear whether those clades form a monophyletic group to the exclusion of Old World Columba, but several analyses produce that result. Species of Old World Columba are closely related to Streptopelia, with species of Now World Columba clustering outside that group. Taxonomic changes suggested by our results include merging Nesoenas with Streptopelia and changing the generic name for Now World Columba species to Patagioenas. Vocal similarities between S. picturata and N. mayeri are striking, given the general diversity of vocalizations in other species. [KEYWORDS: C-14 2-deoxyglucose uptake; collared dove; sex-differences; dna-sequences; ring doves; vocalizations; mitochondrial; evolution; decaocto; risoria]https://doi.org/10.1642/0004-8038(2001)118[0874:AMPOTD]2.0.CO;2Parental correlates of offspring sex ratio in Eurasian Oystercatchers
We investigated hatchling and fledgling sex ratios in Eurasian Oystercatchers (Haematopus ostralegus) using random amplified polymorphic DNA markers. The overall hatchling (53% males, n = 374 hatchlings from 177 broods) and fledgling (49% males, n = 51) sex ratio did not differ significantly from unity. Hatchling and fledgling sex ratios were not correlated with laying date, clutch size, brood size, egg-laying sequence, territory quality male age, or male breeding experience, but hatchling sex ratio was positively correlated with age and breeding experience of females (0.05 <P <0.075, n = 71). Older females produced more sons irrespective of the position of the offspring in the egg-laying sequence. Fledging mass was not correlated with female age, so the Trivers and Willard (1973) hypothesis is unlikely to explain our results. Sons dispersed less than daughters, so the local resource competition hypothesis of Clark (1978) might apply. The adaptive significance of a male-biased sex ratio in clutches produced by older females is speculative because the costs and benefits of dispersing versus philopatric offspring to parents and offspring are largely unknown. [KEYWORDS: Local resource competition; haematopus-ostralegus; monogamous oystercatcher; reproductive success; territory quality; paternal age; birds; selection; population; helpers]https://doi.org/10.1642/0004-8038(2000)117[0980:PCOOSR]2.0.CO;2Offspring sex ratio is related to male body size in the great tit (Parus major)
Sex allocation theory predicts that the allocation of resources to male and female function should depend on potential fitness gain realized through investment in either sex. In the great tit (Parus major), a monogamous passerine bird, male resource-hording potential (RHP) and fertilization success both depend on male body size (e.g., tarsus length) and plumage traits (e.g., breast stripe size). It is predicted that the proportion of sons in a brood should increase both with male body size and plumage traits, assuming that these traits show a father-offspring correlation. This was confirmed in our study: the proportion of sons in the brood increased significantly with male tarsus length and also, though not significantly, with the size of the breast stripe. A sex ratio bias in relation to male tarsus length was already present in the eggs because (1) the bias was similar among broods with and without mortality before the nestlings' sex was determined, and (2) the bias remained significant when the proportion of sons in the clutch was conservatively estimated, assuming that differential mortality before sex determination caused the bias. The bias was still present among recruits. The assumption of a father-offspring correlation was confirmed for tarsus length. Given that both RHP and fertilization success of male great tits depend on body size, and size of father and offspring is correlated, the sex ratio bias may be adaptive. [KEYWORDS: body size, great tits, Parus major, resource holding potential, sex allocation, sexual selection]https://doi.org/10.1093/beheco/10.1.68Ectoparasite infestation and sex-biased local recruitment of hosts
Dispersal patterns of organisms are a fundamental aspect of their ecology, modifying the genetic and social structure of local populations(1-4). Parasites reduce the reproductive success and survival of hosts and thereby exert selection pressure on host life-history traits(4-6), possibly affecting host dispersal(7-9). Here we test experimentally whether infestation by hen fleas, Ceratophyllus gallinae, affects sex- related recruitment of great tit, Parus major, fledglings. Using sex-specific DNA markers, we show that flea infestation led to a higher proportion of male fledglings recruiting in the local population in one year. In infested broods, the proportion of male recruits increased with brood size over a three year period, whereas the proportion of male recruits from uninfested broods decreased with brood size. Natal dispersal distances of recruits from infested nests were shorter than those from uninfested nests(10). To our knowledge, this study provides the first evidence for parasite-mediated host natal dispersal and local recruitment in relation to sex. Current theory needs to consider parasites as potentially important factors shaping life-history traits associated with host dispersal. [KEYWORDS: Great-tits; natal dispersal; parus-major; birds; philopatry competition; adaptation; evolution; survival; systems]https://doi.org/10.1038/21881Sexing birds using random amplified polymorphic DNA (RAPD) markers
We used random amplified polymorphic DNA (RAPD) markers to sex birds from small tissue (usually blood) samples. Arbitrarily chosen 10-mer PCR primers were screened with DNA from known-sex individuals for the production of a bright female-specific band. Suitable primers were found for seven bird species after screening about 30 primers (range 2-63), and no primer was found for three other species after screening about 50 primers for each species. Investigations into the reliability of RAPD markers for sexing great tits Parus major and oystercatchers Haematopus ostralegus show that: (i) when PCR reaction conditions for great tit DNA are varied, either the presence of the female-specific band correctly predicts the individual's sex or no DNA amplification occurs; (ii) the female-specific band in great tits can be sequenced,and subsequently amplified using specific PCR primers; (iii) null alleles of the female- specific fragment occur at an estimated frequency of 0% (n = 241 females) in great tits and 0.6% (n > 290 females) in oystercatchers; (iv) the female-specific fragment in great tits occurs in individuals from a wide geographical range encompassing two subspecies; and (v) the relative intensity of bands in great tit RAPD banding profiles is consistent across individual birds and scorers. The RAPD primers that we have identified are generally species specific, and the consequent time cost of screening for primers is the chief disadvantage of using RAPD markers to sex birds. However, with large sample sizes this disadvantage is outweighed by the relative technical simplicity and low cost of the technique. [KEYWORDS: birds; DNA isolation; null alleles; PCR; RAPD markers; sex determination Arbitrary primers; genetic-markers; w-chromosome; identification; pcr; ratios]https://doi.org/10.1046/j.1365-294x.1998.00331.xParental behaviour is unrelated to experimentally manipulated great tit brood sex ratio
Parental investment may be biased with respect to parental sex or offspring sex or there may be an interaction between parental and offspring sex. We investigated whether any of these types of bias occurred in great tits, Parus major. By sexing chicks using random amplified polymorphic DNA (RAPD) markers and subsequently moving chicks between broods, we were able to manipulate broods early in the nestling period to give all-male, mixed-sex and all-female broods. Provisioning behaviour (total feeding rate, proportion of feeding visits by the male, prey size, visit duration and proportion of visits in which a faecal sac was removed) was measured for broods aged 8- 9 and 11-12 days. Nest defence behaviour was measured for 15- day-old broods. Parental weight, the occurrence of second broods and overwinter survival of the parents were also analysed, There were some differences in parental care between the parents: males made the majority of feeding visits and were more vigorous in nest defence. However, there was no evidence that parental care varied in relation to brood sex ratio. or that there was an interaction in parental tare between parental sex and brood sex ratio. (C) 1998 The Association for the Study of Animal Behaviour. [KEYWORDS: Red-winged blackbirds; parus-major; statistical power; zebra finches; offspring sex; selection; consequences; competition; allocation; dispersal]https://doi.org/10.1006/anbe.1998.0763New CMS types in Plantago lanceolata and their relatedness
Mitochondrial variation in Plantago lanceolata was used to detect new CMS types. Directional reciprocal crosses were made between plants which differed in mtDNA restriction patterns. Differential segregation of male steriles in reciprocal crosses indicated that the parents differed in CMS type. MtDNA variation revealed nine RFLP patterns, which could be categorised according to the sex phenotype of the plants as MS1 (brown-anther type), MS2 (petaloid flower type) and MS3 (more yellow anthers than MS1). A single mtDNA pattern was found within MS1, six mtDNA patterns were found within the MS2 group, and two mtDNA patterns were found within hermaphrodites which segregated MS3 in the crosses. MS1 and MS2 are known to represent different CMS types, CMSI and CMSII. In reciprocal crosses between plants with different mtDNA patterns within the MS2 group, different ratios of male steriles segregated in the crosses, indicating that the parents differed in CMS type. Within the MS2 group two CMS types were found, designated CMSIIa and b. Finally, the sex phenotype H/MS3 turned out to be a different type. From previous studies it was known that the MS3 phenotype can also occur in CMSI and CMSII types, hence it is unclear whether MS3 is diagnostic for CMSIII. Since the data in this study cannot distinguish between the new type being a fully restored new CMS type or a 'Normal' cytoplasm, it was denoted as CMSIII. In total, four CMS types were found in the material studied. CtDNA variation was screened and three chloroplast haplotypes were identified. Two haplotypes were associated with CMSI plants, and one haplotype with the other CMS types. The ctDNA variation indicated that the CMSI type is widespread within the species, due to migration rather than to recurrent mutation. This may lead to the conclusion that only a limited number of CMS types are successful. [KEYWORDS: Plantago lanceolata; gynodioecy; CMS; ctDNA; reciprocal crosses Cytoplasmic male-sterility; mitochondrial-dna; chloroplast dna; intraspecific variation; male-fertility; daucus-carota; plastid dna; inheritance; maize; genome]https://doi.org/10.1007/s001220050449Extreme adaptive modification in sex ratio of the Seychelles warbler's eggs
Young Seychelles warblers Acrocephalus sechellensis often remain in their natal territories as helpers. Helpers on low- quality territories (as measured by food availability) reduce their parents' reproductive success, whereas 1-2 helpers on high-quality territories increase their parents' reproductive success, thereby enhancing their inclusive fitness, in addition to gaining experience(1,2), and opportunities for co- breeding(3). Helpers are mostly females, and we have previously suggested that parents may adjust the sex of their single egg to territory quality(4). We therefore took blood samples from nestlings, and determined sex using random amplified polymorphic DNA (RAPD) markers. We show that biased hatching sex ratios are caused by biased production and not by differential embryo mortality. Unhelped breeding pairs on low- quality territories produce 77% sons, whereas unhelped pairs on high-quality territories produce 13% sons. Breeding pairs that were transferred from low- to high-quality territories switched from the production of male to female eggs. Breeding pairs occupying high-quality territories switched from producing female eggs when no or one helper was present, to producing male eggs when two helpers were present in the territory. [KEYWORDS: Selection; dispersal; helpers; nest]https://doi.org/10.1038/385522a0Low frequency of extra-pair fertilizations in the Great Tit Parus major revealed by DNA fingerprinting
Multilocus DNA fingerprinting was used to estimate the frequency of extra-pair fertilizations in a low density, island population of Great Tits Parus major. A total of 69 pairs and 516 offspring from 82 breeding attempts were examined. Only 18 offspring (3.5%) in seven different nests were not fathered by the attending male. The sample included one brood in which all nine chicks were fathered by an extra-pair male. One chick from a nest of eight was the result of intra-specific brood parasitism. Three chicks from a brood of nine could be matched with the male but not with the female. Observations at this nestbox suggested that mate switching had occurred during the laying period. The percentage of extra-pair fertilizations did not differ between first clutches and (experimentally induced) replacement clutches. Females mated to small males were more likely to have extra-pair young in the nest. Because both extra-pair paternity and intraspecific brood parasitism are rare in this population, a reliable measure of reproductive success can be obtained by counting the number of offspring. [KEYWORDS: Intraspecific brood parasitism; mixed reproductive strategies; conspecific nest parasitism; eastern bluebirds; genetic similarity; female preference; sperm competition; hatching failure; sexual selection; tree swallows]https://doi.org/10.2307/3676974Great tit hatchling sex ratios
The sex of Great Tit Parus major nestlings was determined using PCR RAPDs. Because this technique requires minute amounts of DNA, chicks could be sampled soon (0-2d) after hatching, before any nestling mortality occurred. The proportion of males among 752 chicks hatching in 102 broods (98.9% of those that hatched) increased with hatching date from 42.4% male in first broods (n=555 chicks) to 50.9% male in second broods (n=167). The proportion of males among hatchlings also decreased with increasing clutch size and increased with increasing hatching asynchrony. These three variables are intercorrelated and it was not possible to separate them statistically. Hatchling sex ratio was not correlated with the age, weight or wing-length of either of the parents, brood size at hatching or fledging, hatching or fledging success, mean chick weight, or position in the hatching sequence. The functional significance of the sex ratio variation found is unknown. [KEYWORDS: Red-winged blackbirds; lesser snow geese; egg sequence; parus-major; seasonal-variation; size; identification; consequences; mortality; dispersal]https://doi.org/10.2307/3677142
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Avian blood sample collection
Since 1994, we collect genetic samples from insects (winter moth) and birds (mainly great tit, blue tit, pied flycatcher, oystercatcher and various waterfowl). The location and specifications of a sample can be found in our relational data warehouse. There are more than 170,000 blood samples, feathers and other tissues stored at NIOO. The samples can be used to investigate the genotype of an individual or population in relation to their fenotype.