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van Oers, K.

Publications and source records attributed to van Oers, K..

At least 19 recordsLinked to original sources

City and forest great tits respond differently to artificial light at night: insights from a common garden study

Artificial light at night (ALAN) disrupts the natural light-dark cycle, which is the most important cue for synchronizing circadian clocks. If populations most exposed to ALAN adapt to get less disturbed by it, we expect forest and city populations to differ genetically. We tested this prediction in a common garden experiment using a songbird, the great tit (Parus major), originating from forest and city populations. We simulated ALAN exposure during the breeding season by keeping the birds in pairs under ALAN or dark nights for three months and then repeated the experiment in the following year with the same pairs under the opposite treatment. The advancement of daily onset under ALAN disappeared over time for city birds, but not for their forest counterparts. For these same birds, we measured their onset of daily activity under constant dim light and shift in activity in response to light pulses and showed that the city/forest difference in behavioural response was not reflected in any clock property measured. This indicates that city and forest birds differ genetically in the downstream behavioural response to ALAN, and not in the circadian clock. Thus, urbanization is unlikely to select for divergence in circadian clock properties in songbirds.

evolutionary biology↗

An introgressed haplotype decouples phenotype from genome-wide ancestry

Introgression redistributes genetic variation among diverging lineages, shaping evolution-ary trajectories and contributing to phenotypic evolution. Yet how localized introgressed genomic regions persist despite extensive genomic homogenization remains poorly under-stood. Here, we investigate the evolutionary history of the northeastern Iranian great tit (Parus major intermedius), a grey-plumaged member of the great tit complex occurring at the eastern range margin of the green- and yellow-plumaged major lineage, adjacent to the grey-plumaged Central Asian bokharensis lineage, and long regarded as a putative hybrid. We find that P. m. intermedius retains predominantly major-derived genomic ancestry despite its grey plumage, revealing extensive genomic homogenization across the genome. Surprisingly, a single localized introgressed haplotype on chromosome 24 retains bokharensis-derived ancestry, exhibits elevated genomic differentiation relative to the genomic background, and overlaps the carotenoid-processing gene BCO2, a strong candidate underly-ing plumage pigmentation. Our findings provide a genomic explanation for the discordance between phenotype and genome-wide ancestry, demonstrating how localized introgression can preserve genomic regions associated with phenotypic divergence despite extensive genomic homogenization. This system illustrates how individual genomic regions can retain distinct evolutionary histories long after the surrounding genome has largely homogenized.

evolutionary biology↗

Enemies, more than sex, shape butterfly post-mating odor evolution

Not all odors influencing mating behavior evolve as sex pheromones. Female butterflies post-mating odors have been considered species-specific anti-aphrodisiac pheromones shaped by sexual selection but may also serve broader ecological roles shaped by natural selection. Males transfer odors to females that repel rivals, yet the widespread use of these compounds across phyla makes them targets for eavesdropping, such as by phoretic egg parasitoids. We show that in cabbage white butterflies (Pieris spp.), these odors are highly variable and attract parasitoids, deter predators, and influence oviposition. Using gas chromatography and electroantennography, we demonstrate that odor emission and perception lack species-specificity: compounds once thought unique to P. brassicae and P. rapae are shared across Pieridae. In P. napi, odor variation among populations correlates with parasitoid pressure, but not with latitude, genetic distance, or mating frequency, suggesting ecological rather than sexual drivers. In P. brassicae, CRISPR/Cas9 disruption of odor perception alters oviposition and increases susceptibility to parasitism. Moreover, these odors render females unpalatable to birds. Together, our results show that post-mating odors in Pieris butterflies may act as aposematic signals. We provide evidence that these signals evolve under multiple selective pressures, balancing deterrence of mates and predators, parasitoid avoidance, and host-plant interactions. These findings suggest that chemical signals should be viewed as integrating ecological and reproductive pressures, rather than being interpreted solely through the lens of sexual communication.

ecology↗

Fishing pressure induces changes in DNA methylation in genetically homogeneous marine metapopulations

Trait-selective harvesting by fisheries can impose strong selective pressures on fish populations, driving changes in life history traits affecting fisheries productivity and ecosystem functioning. While the genetic consequences of harvesting have been extensively studied, the extent to which phenotypic variation reflects genomic evolution versus environmentally-induced plasticity remains unclear. Epigenetic mechanisms, such as DNA methylation, may mediate between these processes, serving as a rapid and reversible response to the selective pressures imposed by harvesting. In this study, we implemented an improved laboratory and bioinformatics protocol, epiGBS3, to examine genomic variation and DNA methylation patterns in the marine fish Xyrichtys novacula. The study spanned three replicated geographical areas each comprising two adjacent locations: an intensively exploited fishery and a no-take Marine Protected Area (ntMPA). A nested analysis design across the three areas revealed strong gene flow and no evidence of genetic structure. Nevertheless, nucleotide diversity was significantly reduced in fisheries relative to ntMPAs. We also found that DNA methylation levels differed between protected and exploited sites after controlling for age, suggesting that fishing may influence epigenetic changes independently of fisheries-induced age-truncation effects. This represents one of the first lines of evidence that fisheries can potentially shape epigenetic variation, supporting DNA methylation as contributor to local adaptation under high gene flow and strong anthropogenic selection.

molecular biology↗

Size in the city: morphological differences between city and forest great tits have a genetic basis

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

evolutionary biology↗

Independent avian epigenetic clocks for aging and development

Information on individual age is a fundamental aspect in many ecological and evolutionary studies. However, accurate and non-lethal methods that can be applied to estimate the age of wild animals are often absent. Furthermore, since the process of ageing is accompanied by a physical decline and the deterioration of biological functions, the biological age often deviates from the chronological age. Epigenetic marks are widely suggested to be associated with this age-related physical decline, and especially changes in DNA methylation are suggested to be reliable age-predictive biomarkers. Here, we developed separate epigenetic clocks for ageing for development in a small passerine bird, the great tit (Parus major). The ageing clock was constructed and evaluated using erythrocyte DNA methylation data of 122 post-fledging individuals, and the developmental clock using 67 pre-fledging individuals from a wild population. Using a leave-one-out cross validation approach, we were able to accurately predict the ages of individuals with mediation absolute deviations of 0.40 years for the ageing and 1.06 days for the development clock. Moreover, using existing data from a brood-size manipulation we show that nestlings from reduced broods are estimated to be biologically older compared to control nestlings, while they are expected to have higher fitness. These epigenetic clocks provide further evidence that, as observed in mammals, changes in DNA methylation of certain CpG sites are highly correlated with chronological age in birds and open up new avenues for broad applications in behavioural and evolutionary ecology.

ecology↗

DNA methylation associates with sex-specific effects of experimentally increased yolk testosterone in wild nestlings

Maternal hormones can profoundly impact offspring physiology and behaviour in sex-dependent ways. Yet little is known on the molecular mechanisms linking these maternal effects to offspring phenotypes. DNA methylation, an epigenetic mechanism, is suggested to facilitate maternal androgens effects. To assess whether phenotypic changes induced by maternal androgens associate with DNA methylation changes, we experimentally manipulated yolk testosterone levels in wild great tit eggs (Parus major) and quantified phenotypic and DNA methylation changes in the hatched offspring. Increased yolk testosterone levels decreased the begging probability, emphasised sex-differences in fledging mass and affected methylation at 763 CpG sites, but always in a sex-specific way. These sites associated with genes involved in growth, oxidative stress and reproduction, suggesting sex-specific trade-offs to balance the costs and benefits of exposure to high yolk testosterone levels. Future studies should assess if these effects extend beyond the nestling stage and impact fitness.

molecular biology↗

Continent-wide drivers of spatial synchrony in age structure across wild great tit populations

Spatio-temporal variation in age structure influences population dynamics, yet we have limited understanding of the spatial scale at which its fluctuations are synchronised between populations. Using 32 great tit populations, spanning 3200km and >130,000 birds across 67 years, we quantify spatial synchrony in breeding age structure and its drivers. We show that larger clutch sizes, colder winters and summers, and larger beech crops lead to younger populations. We report distant-dependent spatial synchrony of age structure, which is maintained at approximately 650km. Despite covariation with age structure, reproductive and environmental variables do not influence the scale of synchrony, except for a moderate effect of beech masting. We suggest that local ecological and density-dependent dynamics impact how environmental variation interacts with age structure, influencing estimates of the environments effect on spatial synchrony. Our analyses demonstrate the operation of synchrony in age structure over large scales, with implications for age-dependent demography in populations.

ecology↗

Seasonal and environmental factors contribute to the variation in the gut microbiome: a large-scale study of a small bird

Environmental variation can shape the gut microbiome, but majority of studies use captive-bred species, while data on large-scale variation in the gut microbiome and the associated environmental factors is lacking. Furthermore, previous studies have limited taxonomical coverage, and for example knowledge about avian gut microbiomes is still scarce. We investigated large-scale environmental variation in the gut microbiome of wild adult great tits across the species European distribution range. Our results show that gut microbiome diversity is higher during winter and that there are compositional differences between winter and summer gut microbiomes. During winter, individuals inhabiting mixed forest habitat show higher gut microbiome diversity, whereas there was no similar association during summer. Also, temperature was found to be a small contributor to compositional differences in the gut microbiome. We did not find significant differences in the gut microbiome among populations, nor any association between latitude, rainfall, and the gut microbiome. The results suggest that there is a seasonal change in wild avian gut microbiomes, but that there are still many unknown factors that shape the gut microbiome of wild bird populations.

ecology↗

Parental control: ecology drives plasticity in parental response to offspring signals

Different bird species have completely different parent-offspring interactions. When food is plentiful, the chicks that are begging the loudest are fed the most. When food is scarce, bird species instead feed the largest offspring. While this variation could be due to parents responding to signalling differently based on food availability, it could equally be due to offspring adjusting their behaviour, or to variation in information availability. We tested between these competing explanations experimentally, by manipulating food availability in a population of wild great tits, Parus major, while standardising offspring behaviour and size. We found that when food was more plentiful, parents were: (1) more likely to preferentially feed the chicks that were begging the most; and (2) less likely to preferentially feed larger chicks. In addition, we consistently found these same patterns, in a meta-analysis across 57 bird species. Overall, our results suggest that parents have more control over food distribution than offspring do, and that they flexibly adjust how they respond to both offspring signals and cues of offspring quality in response to food availability. Consequently, depending upon environmental conditions, predictably different signalling systems are favoured.

animal behavior and cognition↗

Reorganization of molecular networks associated with DNA methylation and changes in the rearing environments of the house wren (Troglodytes aedon)

Environmental change, such as increased rates of urbanization, can induce shifts in phenotypic plasticity with some individuals adapting to city life while others are displaced. A key trait that can facilitate adaptation is the degree at which animals respond to stress. This stress response has a heritable component and exhibits intra- and inter-individual variation. However, the mechanisms behind this variability and whether they might be responsible for adaptation to different environments are not known. Variation in DNA methylation can be a potential mechanism that mediates environmental effects on the stress response. We used an inter- and intra-environmental cross-foster experiment to analyze the contribution of DNA methylation to early-life phenotypic variation. We found that at hatching, urban house wren (Troglodytes aedon) offspring had increased methylation as compared to their rural counterparts, and observed plasticity in methylation as offspring aged, indicating developmental effects of the rearing environment on methylation. Differential methylation analyses showed that cellular respiration genes were differentially expressed at hatching and behavioral and metabolism genes were differentially expressed at fledgling. Lastly, hyper-methylation of a single gene (CNTNAP2) is associated with increased glucocorticoid levels. These differential methylation patterns linked to a specific physiological phenotype suggest that DNA methylation may be a mechanism by which individuals adapt to novel environments. Characterizing genetic and environmental influences on methylation is critical for understanding the role of epigenetic mechanisms in evolutionary adaptation.

evolutionary biology↗

No reproductive benefits of dear enemy recognition in a territorial songbird

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.

animal behavior and cognition↗

Artificial light at night shifts the circadian system but still leads to physiological disruption in a wild bird

Globally increasing levels of artificial light at night (ALAN) are associated with shifts in circadian rhythms of behaviour in many wild species. However, it is still unclear whether changes in behavioural timing are underlined by parallel shifts in the molecular clock, and whether such internal shifts may differ between different tissues and physiological pathways, which could highlight circadian disruption. We tackled these questions in a comprehensive study that integrated behavioural, gene expression and metabolomic analyses. We exposed captive male great tits (Parus major) to three ALAN intensities or to dark nights, recorded their activity rhythms and obtained mid-day and midnight samples of brain, liver, spleen and blood. ALAN advanced wake-up time, and this shift was paralleled by an advance in the expression of the clock gene BMAL1 in all tissues, suggesting close links of brain and peripheral clock gene expression with activity rhythms. However, several metabolic and immune genes were desynchronised the shifted BMAL1 expression, suggesting circadian disruption of behaviour and physiology. This result was reinforced by untargeted metabolomic profiling, which showed that only 9.7% of the 755 analysed metabolites followed the behavioural shift. We suggest circadian as a key mediator of the health impacts of ALAN on wild animals.

zoology↗

Does arsenic contamination affect DNA methylation patterns in a wild bird population? An experimental approach

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 is 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 post-natal 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 phenomena in polluted populations, and what the consequences are for organism functioning and for population dynamics.

ecology↗

epiGBS2: an improved protocol and automated snakemake workflow for highly multiplexed reduced representation bisulfite sequencing

epiGBS is an existing reduced representation bisulfite sequencing method to determine cytosine methylation and genetic polymorphisms de novo. Here, we present epiGBS2, an improved epiGBS laboratory protocol and user-friendly bioinformatics pipeline for a wide range of species with or without reference genome. epiGBS2 decreases costs and time investment and increases user-friendliness and reproducibility. The library protocol was adjusted to allow for a flexible choice of restriction enzymes and a double digest. Instead of fully methylated adapters, semi-methylated adapters are now used. The bioinformatics pipeline was improved in speed and integrated in the snakemake workflow management system, which now makes the pipeline easy to execute, modular, and parameter settings flexible. We also provide a detailed description of the laboratory protocol, 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.3819996), and example output.

bioinformatics↗

Epigenetic mediation of the onset of reproduction in a songbird

Climate change significantly impacts natural populations, particularly phenology traits, like the seasonal onset of reproduction in birds. This impact is mainly via plastic responses in phenology traits to changes in the environment, but the molecular mechanism mediating this plasticity remains elusive. Epigenetic modifications can mediate plasticity and consequently constitute promising candidates for mediating phenology traits. Here, we used genome-wide DNA methylation profiles of individual great tit (Parus major) females that we blood sampled repeatedly throughout the breeding season. We demonstrate rapid and directional variation in DNA methylation within the regulatory region of genes known to play key roles in avian reproduction that are in line with observed changes in gene expression in chickens. Our findings provide an important step towards unraveling the molecular mechanism mediating a key life history trait, an essential knowledge-gap for understanding how natural populations may cope with future climate change. IMPACT SUMMARYNatural populations are increasingly challenged by changing environmental conditions like global increases in temperature. A key way for species to adapt to global warming is via phenotypic plasticity, i.e. the ability to adjust the expression of traits to the environment. We, however, know little about how the environment can interact with an organisms genetic make-up to shape its trait value. Epigenetic marks are known to vary with the environment and can modulate the expression of traits without any change in the genetic make-up and therefore have the potential to mediate phenotypic plasticity. To study the role of epigenetics for phenotypic plasticity, we here focus on the great tit (Parus major), a species that is strongly affected by global warming and plastic for temperature in an essential phenology trait, the seasonal onset of egg laying. As a first step, we investigated whether great tit females show within-individual and short-term variation in DNA methylation that corresponds to changes in the reproductive state of females. We therefore housed breeding pairs in climate-controlled aviaries to blood sample each female repeatedly throughout the breeding season and used these repeated samples for methylation profiling. We found rapid and directional variation in DNA methylation at the time females prepared to initiate egg laying that is located within the regulatory region of genes that have previously described functions for avian reproduction. Although future work is needed to establish a causal link between the observed temporal variation in DNA methylation and the onset of reproduction in female great tits, our work highlights the potential role for epigenetic modifications in mediating an essential phenology trait that is sensitive to temperatures.

ecology↗

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

Anthropogenic pollution is known to negatively influence an organisms physiology, behavior and fitness. Epigenetic regulation, such as DNA methylation, has been hypothesized as one 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 lead at environmentally relevant levels. Secondly, we studied the effects of heavy metal exposure in a population close to a copper smelter, where birds suffer from pollution-related decrease in food quality. For both comparisons, the analysis of about million CpGs covering most of the annotated genes, revealed that regions enriched for developmental processes showed pollution-related changes in DNA methylation, but the results were not consistent with binomial and beta binomial regression. Our study indicates that post-natal anthropogenic heavy metal exposure can affect methylation levels of development related genes in a wild bird population.

molecular biology↗

The great tit HapMap project: a continental-scale analysis of genomic variation in a songbird

A major aim of evolutionary biology is to understand why patterns of genomic diversity vary among populations and species. Large-scale genomic studies of widespread species are useful for studying how the environment and demographic history shape patterns of genomic divergence, and with the continually decreasing cost of sequencing and genotyping, such studies are now becoming feasible. Here, we carry out one of the most geographically comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit (Parus major) HapMap project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning almost the entire geographic range of the European great tit subspecies. We found that genome-wide variation was consistent with a recent colonisation across Europe from a single refugium in South-East Europe, with bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly heterogeneous, with clear "islands of differentiation" even among populations with very low levels of genome-wide differentiation. Low local recombination rate in the genome was a strong predictor of high local genomic differentiation (FST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination is a key driver of highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, most likely as a result of recent directional selection at the range edges of this species. Haplotype-based measures of selection were also related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. These regions under positive selection contained candidate genes associated with morphology, thermal adaptation and colouration, providing promising avenues for future investigation. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into evolution.

evolutionary biology↗