Kees van Oers

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

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

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

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

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

Personalities are general properties of humans and other animals. Different personality traits are phenotypically correlated, and heritabilities of personality traits have been reported in humans and various animals. In great tits, consistent heritable differences have been found in relation to exploration, which is correlated with various other personality traits. In this paper, we investigate whether or not risk–taking behaviour is part of these avian personalities. We found that (i) risk–taking behaviour is repeatable and correlated with exploratory behaviour in wild–caught hand–reared birds, (ii) in a bi–directional selection experiment on ‘fast’ and ‘slow’ early exploratory behaviour, bird lines tend to differ in risk–taking behaviour, and (iii) within–nest variation of risk–taking behaviour is smaller than between–nest variation. To show that risk–taking behaviour has a genetic component in a natural bird population, we bred great tits in the laboratory and artificially selected ‘high’ and ‘low’ risk–taking behaviour for two generations. Here, we report a realized heritability of 19.3±3.3% (s.e.m.) for risk–taking behaviour. With these results we show in several ways that risk–taking behaviour is linked to exploratory behaviour, and we therefore have evidence for the existence of avian personalities. Moreover, we prove that there is heritable variation in more than one correlated personality trait in a natural population, which demonstrates the potential for correlated evolution.

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

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

Phenology, seasonal timing and circannual rhythms: towards a unified framework

Phenology refers to the periodic appearance of life-cycle events and currently receives abundant attention as the effects of global change on phenology are so apparent. Phenology as a discipline observes these events and relates their annual variation to variation in climate. But phenology is also studied in other disciplines, each with their own perspective. Evolutionary ecologists study variation in seasonal timing and its fitness consequences, whereas chronobiologists emphasize the periodic nature of life-cycle stages and their underlying timing programmes (e.g. circannual rhythms). The (neuro-) endocrine processes underlying these life-cycle events are studied by physiologists and need to be linked to genes that are explored by molecular geneticists. In order to fully understand variation in phenology, we need to integrate these different perspectives, in particular by combining evolutionary and mechanistic approaches. We use avian research to characterize different perspectives and to highlight integration that has already been achieved. Building on this work, we outline a route towards uniting the different disciplines in a single framework, which may be used to better understand and, more importantly, to forecast climate change impacts on phenology.

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

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

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

Polymorphisms in the dopamine receptor D4 gene (DRD4) have been related to individual variation in novelty‐seeking or exploratory behaviour in a variety of animals, including humans. Recently, the human DRD4 orthologue was sequenced in a wild bird, the great tit (Parus major) and a single nucleotide polymorphism in exon 3 of this gene (SNP830) was shown to be associated with variation in exploratory behaviour of lab‐raised individuals originating from a single wild population. Here we test the generality of this finding in a large sample of free‐living individuals from four European great tit populations, including the originally sampled population. We demonstrate that the association between SNP830 genotype and exploratory behaviour also exists in free‐living birds from the original population. However, in the other three populations we found only limited evidence for an association: in two populations the association appeared absent; while in one there was a nonsignificant tendency. We could not confirm a previously demonstrated interaction with another DRD4 polymorphism, a 15 bp indel in the promoter region (ID15). As yet unknown differences in genetic or environmental background could explain why the same genetic polymorphism (SNP830) has a substantial effect on exploratory behaviour in one population, explaining 4.5–5.8% of the total variance—a large effect for a single gene influencing a complex behavioural trait—but not in three others. The confirmation of an association between SNP830 genotype and personality‐related behaviour in a wild bird population warrants further research into potential fitness effects of the polymorphism, while also the population differences in the strength of the association deserve further investigation. Another important future challenge is the identification of additional loci influencing avian personality traits in the wild.

Personality predicts the use of social information

The use of social information is known to affect various important aspects of an individuals 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.

Genome‐wide SNP detection in the great tit Parus major using high throughput sequencing

Identifying genes that underlie ecological traits will open exiting possibilities to study gene–environment interactions in shaping phenotypes and in measuring natural selection on genes. Evolutionary ecology has been pursuing these objectives for decades, but they come into reach now that next generation sequencing technologies have dramatically lowered the costs to obtain the genomic sequence information that is currently lacking for most ecologically important species. Here we describe how we generated over 2 billion basepairs of novel sequence information for an ecological model species, the great tit Parus major. We used over 16 million short sequence reads for the de novo assembly of a reference sequence consisting of 550 000 contigs, covering 2.5% of the genome of the great tit. This reference sequence was used as the scaffold for mapping of the sequence reads, which allowed for the detection of over 20 000 novel single nucleotide polymorphisms. Contigs harbouring 4272 of the single nucleotide polymorphisms could be mapped to a unique location on the recently sequenced zebra finch genome. Of all the great tit contigs, significantly more were mapped to the microchromosomes than to the intermediate and the macrochromosomes of the zebra finch, indicating a higher overall level of sequence conservation on the microchromosomes than on the other types of chromosomes. The large number of great tit contigs that can be aligned to the zebra finch genome shows that this genome provides a valuable framework for large scale genetics, e.g. QTL mapping or whole genome association studies, in passerines.

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

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