Droevendaalsesteeg 10
6708 PB Wageningen
The Netherlands
About
The aim of my PhD project is to identify genetic and environmental control mechanism underlying genome-wide DNA methylation and possible functional consequences of gene methylation for natural variation in great tit personality.
Biography
Bernice Sepers (1991) studied Biology (Bachelor of Science) and Environmental Biology (specialisation programme Behavioural Ecology, Master of Science) at Utrecht University. During her major internship at Stichting AAP, she studied the effect of intervention on the abnormal behaviour of ex-laboratory chimpanzees. In her final year she visited the Nova Scotia Department of Natural Resources in Canada to study the environmental conditions that influenced snowmobile trail use by coyotes within lynx home ranges at Cape Breton Island (Nova Scotia, Canada). Her master thesis consisted of an extensive literature review on the effect of epigenetic changes on the behaviour of animals in natural populations (NIOO-KNAW). Bernice graduated in 2016, after which she was funded by a Startersbeurs to study the effect of experimental brood size manipulation on DNA methylation and exploratory behaviour in the great tit at the NIOO-KNAW. After this, she worked as a soil consultant and ecologist at Antea Group (the Netherlands) before starting her PhD at the NIOO-KNAW in 2018. This PhD project focuses on the epigenetics of animal personality, in particular DNA methylation and its influence on exploratory behaviour in great tits. By using established selection lines of fast and slow exploratory birds and several long-term natural populations, this projects aims to identify genetic and environmental control mechanism underlying genome-wide DNA methylation and possible functional consequences of gene methylation for natural variation in great tit personality.
Research groups
CV
Publications
Peer-reviewed publications
The epigenetics of animal personality
https://doi.org/10.1016/j.neubiorev.2023.105194Animal personality, consistent individual differences in behaviour, is an important concept for understanding how individuals vary in how they cope with environmental challenges. In order to understand the evolutionary significance of animal personality, it is crucial to understand the underlying regulatory mechanisms. Epigenetic marks such as DNA methylation are hypothesised to play a major role in explaining variation in phenotypic changes in response to environmental alterations. Several characteristics of DNA methylation also align well with the concept of animal personality. In this review paper, we summarise the current literature on the role that molecular epigenetic mechanisms may have in explaining personality variation. We elaborate on the potential for epigenetic mechanisms to explain behavioural variation, behavioural development and temporal consistency in behaviour. We then suggest future routes for this emerging field and point to potential pitfalls that may be encountered. We conclude that a more inclusive approach is needed for studying the epigenetics of animal personality and that epigenetic mechanisms cannot be studied without considering the genetic background.
Winter food selection and exploratory behavior vary with natal territory characteristics in wild great tits
https://doi.org/10.1007/s00265-023-03335-5Abstract: Differences in habitat characteristics experienced during rearing associate with variation in a range of behavioral phenotypes such as exploratory behavior, foraging behavior and food selection. The habitat-dependent selection hypothesis predicts that animals develop behavioral characteristics fitted to their rearing environment. Yet, little is known about how habitat characteristics during rearing shape how animals face winter conditions and adjust their winter foraging behavior. The aim of this study was to explore how fine-scale rearing habitat characteristics associate with exploratory behavior, food selection, and foraging performance during winter. For this, we measured habitat characteristics during the breeding season in territories of wild great tits (Parus major) and tested first-year juvenile birds that fledged from these territories for exploratory and foraging behavior at feeders during winter. We found evidence that faster explorers were raised in territories with lower quality habitat characteristics. In addition, fast exploring fledglings visited the feeders significantly more (total visits). Moreover, the rearing environment, via caterpillar availability and tree species composition, determined diet selection during winter in first-year birds. These results show support for the habitat-dependent selection hypothesis, since exploratory behavior as well as food selection during winter associate with habitat features of the rearing territories during development. This pattern can be caused either by the kinds of natural foods prevalent during rearing at these sites or because of intrinsic individual differences. Further experiments are needed to disentangle these two. Significance statement: Individuals vary in how they behaviorally adapt foraging and food selection strategies to the environmental conditions. A number of studies have shown that animals develop behavioral characteristics fitted to their rearing environment. However, how habitat characteristics during rearing shape the foraging strategy that animals use to face winter conditions is still unknown. We studied these links in yearling great tits using automated feeders that recorded their visits during winter. Fledglings with a higher exploratory score were born in territories with lower quality habitat characteristics and visited the feeders more. Furthermore, we found an association between caterpillar availability and tree species composition in the rearing territory of juveniles and their subsequent food selection in winter. Our study indicates that certain environmental conditions might favor the development of particular behaviors in birds and that early nutrition could shape food choice later in life.
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.16973Variation in DNA methylation in avian nestlings is largely determined by genetic effects
As environmental fluctuations are becoming more common, organisms need to rapidly adapt to anthropogenic, climatic, and ecological changes. Epigenetic modifications and DNA methylation in particular provide organisms with a mechanism to shape their phenotypic responses during development. Studies suggest that environmentally induced DNA methylation might allow for adaptive phenotypic plasticity that could last throughout an organism's lifetime. Despite a number of studies demonstrating environmentally induced DNA methylation changes, we know relatively little about what proportion of the epigenome is affected by environmental factors, rather than being a consequence of genetic variation. In the current study, we use a partial cross-foster design in a natural great tit (Parus major) population to disentangle the effects of common origin from common rearing environment on DNA methylation. We found that variance in DNA methylation in 8,315 CpG sites was explained by a common origin and only in 101 by a common rearing environment. Subsequently, we mapped quantitative trait loci for the brood of origin CpG sites and detected 754 cis and 4,202 trans methylation quantitative trait loci, involving 24% of the CpG sites. Our results indicate that the scope for environmentally induced methylation marks independent of the genotype is limited and that the majority of variation in DNA methylation early in life is determined by genetic factors instead. These findings suggest that there may be little opportunity for selection to act on variation in DNA methylation. This implies that most DNA methylation variation likely does not evolve independently of genomic changes.https://doi.org/10.1093/molbev/msad086An ecologist's guide for studying DNA methylation variation in wild vertebrates
https://doi.org/10.1111/1755-0998.13624The 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.
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).
Epigenetics and Early Life Stress: Experimental Brood Size Affects DNA Methylation in Great Tits (Parus major)
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.2021.609061Epigenetics of animal personality
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/icaa138Avian ecological epigenetics: pitfalls and promises
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
Popular-scientific publications
Bedelende vrouwtjes
De afgelopen dagen heb ik buiten veel bedelende koolmeesvrouwtjes gehoord. De eerste keer was ik nogal verbaasd, want deze bedelroep lijkt erg op die van net uitgevlogen jonge koolmezen. Jonge koolmezen in april, huh??Kuuk is geringd!
Gisteren was een spannende dag, want Kuuk werd geringd! En tot onze grote vreugde zat vrouw ook in de kast. Lees verder voor het uitgebreide verslag en, uiteraard, de mooie foto’s.Aan de veren kent men de vogel
Kuuk ziet er tot nu toe nog vooral uit als een wit bolletje, maar hier komt langzaam verandering in. We zien dat de veren zich al aan het ontwikkelen zijn, kijkt u maar eens naar de pinnetjes en kwastjes op de vleugels.Hoera, het eerste koolmees ei!
Hoera! Het eerste koolmees ei is gelegd! Rond kwart voor 7 ’s ochtend zien we hoe in nestkast1 een ei wordt gelegd. Zoals het een goede moeder betaamt, dekt mevrouw koolmees haar ei meteen toe.Geheimtaal
Afgelopen maandag ben ik weer het bos in geweest voor een avondcontrole. We zagen al wat nestbouw in veel nestkastjes, net zoals in onze Beleef de Lente nestkasten. Maar wat doen we hiermee? Noteren we dat?Vrouw (nog) op dieet?
Kuuk is nu 11 dagen oud. Aangezien dit mijn eerste jaar is bij team bosuil, is er iedere dag nog genoeg waar ik mij over verwonder. Zo verwonder ik mij over het feit dat mevrouw bosuil zo weinig eet, maar daar lijkt langzaam maar zeker verandering in te komen.Welkom koolmezen Cam2!
Op maandag 18 maart is een extra nestkast aan de koolmeespagina toegevoegd (Cam2). Deze nestkast hangt ook in Dongen en is eigenlijk bedoeld voor spreeuwen. Dat lijkt de koolmezen niet te deren, want er wordt al flink gebouwd in deze nestkast.Muizenkerkhof
Wat doet familie bosuil het toch goed. We kunnen zien dat we hier met ervaren ouders te maken hebben, misschien zelfs een beetje te ervaren?Persoonlijkheid en koolmezen
Ik ben erg blij om te zien dat meneer en mevrouw koolmees de nestkast vaak bezoeken en dat er vaak in geslapen wordt. Zoals Peter al schreef, zijn wij van het NIOO-KNAW tijdens onze avondcontroles ook blij dat koolmezen in nestkasten slapen. In deze blog zal ik hier iets meer over vertellen.Na regen komt zonneschijn
Ook vandaag is weer een dag aangebroken waarop nog geen kuiken te zien is. Gezien de weersomstandigheden is het misschien niet zo’n slecht idee van het kuiken om nog wat langer in het ei te blijven zitten.Bijzondere nestlocaties
Afgelopen weekend zagen we twee vechtende koolmezen in de nestkast. De nestkast is dus erg in trek, toch kan er maar één winnen. De koolmees die aan het kortste eind trekt zal een andere plek moeten vinden om een nestje te bouwen, maar wat zijn de mogelijkheden?Alerte moeder: overdreven of terecht?
Gisteren heeft Emil een leuk filmpje geplaatst waarin te zien is hoe mevrouw bosuil schrikt van een eekhoorn. Gezien de hoeveelheid kleine zoogdieren die meneer bosuil aanvoert, zou je denken dat de bosuil niets te vrezen heeft en juist enkel andere dieren schrik aanjaagt. Is dit ook zo?De perfecte woning
De koolmees broedt van nature in natuurlijke holtes. In Nederland zijn relatief weinig oude bomen met holtes, dus daarom maakt de koolmees graag gebruik van nestkasten. Echter, een koolmees zal niet zomaar iedere nestkast gebruiken.In één keer doorslikken
In de blog van Sharon en het filmpje van Emil hebben we kunnen lezen en zien dat in één van de eieren waarschijnlijk een deuk zit. Het voelt als een déjà vu, ook in 2017 was er een kapot ei. Wat de gevolgen ook zullen zijn, we laten ons niet tegenhouden om van de bosuilen te blijven genieten.Het verleden en de toekomst van onze slaper
De afgelopen dagen zag team koolmees een aantal vragen in de chat voorbij komen. Heeft de koolmees de hele winter in deze nestkast geslapen? Broedde de koolmees al eerder in deze nestkast? Is het te vroeg voor nestbouw? In deze blog ga ik deze prangende vragen beantwoorden.Eindelijk: de bosuilen kunnen bewonderd worden!
Eindelijk is het zover! De bosuilen in Limburg kunnen bewonderd worden! Team bosuil kon de afgelopen dagen al stiekem achter de schermen meekijken en wat was er veel te zien. In deze blog stel ik mijzelf kort voor en breng ik jullie op de hoogte van de laatste belevenissen in en rondom de nestkast.
Projects & collaborations
Projects
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Epigenetics of animal personality: DNA methylation and its influence on exploratory behaviour in great tits
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.
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Thesis defence Bernice Sepers: the role of DNA methylation variation in avian personality
On 28 October, Bernice Sepers (Animal Ecology) will defend her thesis on 'Behavioural epigenetics: insights into the role of heritable and induced DNA methylation variation in avian personality' at Wageningen UR.