Search

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.

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.

Chromosome inversions have clear effects on genome evolution and have been associated with speciation, adaptation and the evolution of the sex chromosomes. In birds, these inversions may play an important role in hybridization of species and disassortative mating. We identified a large (≈64 Mb) inversion polymorphism in the great tit (Parus major) that encompasses almost 1,000 genes and more than 90% of Chromosome 1A. The inversion occurs at a low frequency in a set of over 2,300 genotyped great tits in the Netherlands with only 5% of the birds being heterozygous for the inversion. In an additional analysis of 29 resequenced birds from across Europe we found two heterozygotes. The likely inversion breakpoints show considerable genomic complexity, including multiple copy number variable segments. We identified different haplotypes for the inversion, which differ in the degree of recombination in the center of the chromosome. Overall, this remarkable genetic variant is widespread among distinct great tit populations and future studies of the inversion haplotype, including how it affects the fitness of carriers, may help to understand the mechanisms that maintain it.

Early developmental effects and environmental conditions experienced by parents affect personality traits, even over multiple generations. Yet, the mechanisms underlying transgenerational regulation remain unknown, while determining them is crucial to understand how development affects heritable traits in evolutionary processes. A likely mechanism involved in such epigenetic regulation is DNA methylation, since this can stably alter gene expression in response to environmental factors without structural modifications of the DNA sequence. We study this by associating DNA methylation to variation in exploratory behaviour in the great tit (Parus major). In order to do this, we manipulated brood size in a natural study population. We found more differentially methylated sites in the treatment set (enlarged vs. reduced brood size) than in the control set (control1 versus control2). Furthermore, we found differences in methylation percentage for genes related to growth and behaviour. Therefore, early life stress directly affects epigenetic factors related to growth and behaviour. In the future, we will assess if there is an effect of the observed methylation changes on variation in personality traits, if there is a genetic basis for (personality-related) DNA methylation and if gene methylation variation associates with behaviour and life-history traits under natural conditions.

Background: A widely used approach in next-generation sequencing projects is the alignment of reads to a reference genome. Despite methodological and hardware improvements which have enhanced the efficiency and accuracy of alignments, a significant percentage of reads frequently remain unmapped. Usually, unmapped reads are discarded from the analysis process, but significant biological information and insights can be uncovered from these data. We explored the unmapped DNA (normal and bisulfite treated) and RNA sequence reads of the great tit (Parus major) reference genome individual. From the unmapped reads we generated de novo assemblies, after which the generated sequence contigs were aligned to the NCBI non-redundant nucleotide database using BLAST, identifying the closest known matching sequence. Results: Many of the aligned contigs showed sequence similarity to different bird species and genes that were absent in the great tit reference assembly. Furthermore, there were also contigs that represented known P. major pathogenic species. Most interesting were several species of blood parasites such as Plasmodium and Trypanosoma. Conclusions: Our analyses revealed that meaningful biological information can be found when further exploring unmapped reads. For instance, it is possible to discover sequences that are either absent or misassembled in the reference genome, and sequences that indicate infection or sample contamination. In this study we also propose strategies to aid the capture and interpretation of this information from unmapped reads.

Seasonal timing of reproduction is an important fitness trait in many plants and animals but the underlying molecular mechanism for this trait is poorly known. DNA methylation is known to affect timing of reproduction in various organisms and is therefore a potential mechanism also in birds. Here we describe genome wide data aiming to detect temporal changes in methylation in relation to timing of breeding using artificial selection lines of great tits (Parus major) exposed to contrasting temperature treatments. Methylation levels of DNA extracted from erythrocytes were examined using reduced representation bisulfite sequencing (RRBS). In total, we obtained sequencing data from 63 libraries over four different time points from 16 birds with on average 20 million quality filtered reads per library. These data describe individual level temporal variation in DNA methylation throughout the breeding season under experimental temperature regimes and provides a resource for future studies investigating the role of temporal changes in DNA methylation in timing of reproduction.

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

For over 50 years, the great tit (Parus major) has been a model species for research in evolutionary, ecological and behavioural research; in particular, learning and cognition have been intensively studied. Here, to provide further insight into the molecular mechanisms behind these important traits, we de novo assemble a great tit reference genome and whole-genome re-sequence another 29 individuals from across Europe. We show an overrepresentation of genes related to neuronal functions, learning and cognition in regions under positive selection, as well as increased CpG methylation in these regions. In addition, great tit neuronal non-CpG methylation patterns are very similar to those observed in mammals, suggesting a universal role in neuronal epigenetic regulation which can affect learning-, memory- and experience-induced plasticity. The high-quality great tit genome assembly will play an instrumental role in furthering the integration of ecological, evolutionary, behavioural and genomic approaches in this model species.

International audience

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

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

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

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

Personality traits can be favoured by both natural and artificial selection, if they result in increased fitness or productivity, and therefore play an important role in both wild and domestic populations. Here, we review how personality traits affect and are affected by natural and artificial selection by focusing on studies from both wild and domestic bird populations. Further, we will also explore how artificial selection affects personality and fitness traits in a domestic population. We will use the great tit (Parus major) and the laying hen (Gallus gallus domesticus) as our model species. When comparing the studies on behaviour genetics in great tits and laying hens, it is fascinating to see that two fields of study that seem quite far apart have so much in common.

The use of social information is known to affect various important aspects of an individual’s ecology, such as foraging, dispersal and space use and is generally assumed to be entirely flexible and context dependent. However, the potential link between personality differences and social information use has received little attention. In this study, we studied whether use of social information was related to personality, using barnacle geese, Branta leucopsis, where boldness is a personality trait known to be consistent over time. We found that the use of social information decreased with increasing boldness score of the individuals. Individuals had lower feeding times when they did not follow the social information and this effect was unrelated to boldness score. When manipulating social information, thereby making it incorrect, individuals irrespective of their boldness score, learned that it was incorrect and ignored it. Our results show that social information use depends on the personality type of an individual, which calls for incorporation of these personality-related differences in studies of spatial distribution of animals in which social information use plays a role.

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

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

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

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

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

The integration and synthesis of the data in different areas of science is drastically slowed and hindered by a lack of standards and networking programmes. Long-term studies of individually marked animals are not an exception. These studies are especially important as instrumental for understanding evolutionary and eco-logical processes in the wild. Furthermore, their number and global distribution provides a unique opportunity to assess the generality of patterns and to address broad-scale global issues (e.g. climate change)., To solve data integration issues and enable a new scale of ecological and evolution-ary research based on long-term studies of birds, we have created the SPI-Birds Network and Database (www.spibirds.org)—a large-scale initiative that connects data from, and researchers working on, studies of wild populations of individually recognizable (usually ringed) birds. Within year and a half since the establishment, SPI-Birds has recruited over 120 members, and currently hosts data on almost 1.5 million individual birds collected in 80 populations over 2,000 cumulative years, and counting., SPI-Birds acts as a data hub and a catalogue of studied populations. It prevents data loss, secures easy data finding, use and integration and thus facilitates collab-oration and synthesis. We provide community-derived data and meta-data stand-ards and improve data integrity guided by the principles of Findable, Accessible, Interoperable and Reusable (FAIR), and aligned with the existing metadata lan-guages (e.g. ecological meta-data language)., The encouraging community involvement stems from SPI-Bird's decentralized ap-proach: research groups retain full control over data use and their way of data management, while SPI-Birds creates tailored pipelines to convert each unique data format into a standard format. We outline the lessons learned, so that other communities (e.g. those working on other taxa) can adapt our successful model. Creating community-specific hubs (such as ours, COMADRE for animal demogra-phy, etc.) will aid much-needed large-scale ecological data integration., The SPI-Birds have been supported by an NWO personal grant (grant number 016.Veni.181.054) to A.C., and a Research Council of Norway grant: 223257 (SFF-III) and 267511 (EVOCLIM).