Low heritability of social phenotypes in a nonpasserine waterbird.

Most behavioral traits are known to be weakly heritable, possibly due to their extreme complexity and flexibility. Despite this general pattern, within-species variation in avian colony size choice has been reported to have a strong additive genetic component, but we are aware of no attempts to assess the heritability of avian sociality at the finer spatial scale. Here, we used an animal model and parent-offspring regression to quantify additive genetic variance in social phenotype (local nesting density) in a nonpasserine waterbird, the common tern Sterna hirundo. For this purpose, we used a novel experimental framework, where variation in the social environment was generated by providing birds with artificial patches of attractive nesting substrate that markedly varied in size. During 2011-2019, we collected data on social preferences for either low or high nesting density in over 250 individuals, either kin (mostly parent-offspring relationships) or non-kin recorded breeding multiple times across years. All heritability estimates of local nesting density were low (<0.10), irrespectively of fixed effects (sex and year) included in the models, data used in the modeling (all individuals vs. early recruits), or methodological approach (animal model vs. parent-offspring regression). We conclude that avian sociality, as measured at the local scale, may be much less heritable than colony size choice, as measured at the landscape level. Our study adds to the understanding of additive genetic variance in avian behavior, and it underlines a scale dependency in the heritability of behavioral traits.

Stopover habitat selection drives variation in the gut microbiome composition and pathogen acquisition by migrating shorebirds.

Long-distance host movements play a major regulatory role in shaping microbial communities of their digestive tract. Here, we studied gut microbiota composition during seasonal migration in five shorebird species (Charadrii) that use different migratory (stopover) habitats. Our analyses revealed significant interspecific variation in both composition and diversity of gut microbiome, but the effect of host identity was weak. A strong variation in gut microbiota was observed between coastal and inland (dam reservoir and river valley) stopover habitats within species. Comparisons between host age classes provided support for an increasing alpha diversity of gut microbiota during ontogeny and an age-related remodeling of microbiome composition. There was, however, no correlation between microbiome and diet composition across study species. Finally, we detected high prevalence of avian pathogens, which may cause zoonotic diseases in humans (e.g. Vibrio cholerae) and we identified stopover habitat as one of the major axes of variation in the bacterial pathogen exposure risk in shorebirds. Our study not only sheds new light on ecological processes that shape avian gut microbiota, but also has implications for our better understanding of host-pathogen interface and the role of birds in long-distance transmission of pathogens.

Urbanization is associated with non-coding polymorphisms in candidate behavioural genes in the Eurasian coot.

Extensive transformation of natural land cover into urbanized areas enhances accumulation of phenotypic differences between animals from urban and nonurban populations, but there is little information on whether these changes, especially in terms of animal behaviour and circadian rhythm, have a genetic basis. The aim of this study was to investigate genetic background of behavioural differences between four pairs of urban and nonurban populations of a common waterbird, the Eurasian coot Fulica atra. For this purpose, we quantified polymorphisms in personality-related candidate genes, previously reported to be associated with avian circadian rhythms and behavioural traits that may be crucial for urban life. We found general associations between landscape urbanization level and polymorphisms in 3'UTR region of CREB1 gene encoding transcriptional factor, which participates in development of cognitive functions and regulation of circadian rhythm. We also found significant differentiation between urban and nonurban populations in the intronic region of CKIɛ gene responsible for regulation of circadian clock. Although we lacked evidence for linkage of this intronic variation with coding polymorphisms, genetic differentiation between urban populations was significantly stronger at CKIɛ intron compared with neutral microsatellite markers, suggesting possible local adaptations of CKIɛ expression regulation to specific urban sites. Our results indicate that behavioural differentiation between urban and nonurban coot populations may be the effect of habitat-specific selective pressure resulting in genetic adaptations to urban environment and supporting the microevolutionary scenario. These adaptations, however, prevailed in non-coding regulatory rather than coding gene regions and showed either general or local patterns, revealing high complexity of associations between behaviour and landscape urbanization in birds.

Evolution of innate and adaptive immune genes in a non-model waterbird, the common tern.

Toll-like receptors (TLRs) and the Major Histocompatibility Complex (MHC) are the key pathogen-recognition genes of vertebrate immune system and they have a crucial role in the initiation of innate and adaptive immune response, respectively. Recent advancements in sequencing technology sparked research on highly duplicated MHC genes in non-model species, but TLR variation in natural vertebrate populations has remained little studied and comparisons of polymorphism across both TLRs and MHC are scarce. Here, we aimed to compare variation across innate (four TLR loci) and adaptive (MHC class I and class II) immune genes in a non-model avian species, the common tern Sterna hirundo. We detected relatively high allelic richness at TLR genes (9-48 alleles per locus), which was similar to or even higher than the estimated per locus allelic richness at the MHC (24-30 alleles at class I and 13-16 alleles at class II under uniform sample sizes). Despite this, the total number of MHC alleles across all duplicated loci (four class I and three class II) was much higher and MHC alleles showed greater sequence divergence than TLRs. Positive selection targeted relatively more sites at the MHC than TLRs, but the strength of selection (dN/dS ratios) at TLRs was higher when compared to MHC class I. There were also differences in the signature of positive selection and recombination (gene conversion) between MHC class I and II (stronger signature at class II), suggesting that mechanisms maintaining variation at the MHC may vary between both classes. Our study indicates that allelic richness of both innate and adaptive immune receptors may be maintained at relatively high levels in viable avian populations and we recommend a transition from the traditional gene-specific to multi-gene approach in studying molecular evolution of vertebrate immune system.

Immunocompetent birds choose larger breeding colonies.

Optimal size of social groups may vary between individuals, depending on their phenotypic traits, such as dominance status, age or personality. Larger social groups often enhance transmission rates of pathogens and should be avoided by individuals with poor immune defences. In contrast, more immunocompetent individuals are expected to take advantage of larger group sizes (e.g. better protection, information transfer) with smaller extra costs from pathogen or parasite pressure. Here, we hypothesized that immunocompetence may be a key determinant of group size choice and tested this hypothesis in a colonial waterbird, the common tern Sterna hirundo. We used a unique experimental framework, where formation of breeding colonies of different sizes was induced under uniform environmental conditions. For this purpose, different-size patches of attractive nesting substrate (artificial floating rafts) were provided at a single site with limited availability of natural nesting habitat. Colony size was identified as the only significant predictor of both innate (natural antibody-mediated complement activation) and adaptive (immunoglobulin concentrations) immunological traits in the common terns, as more immunocompetent birds settled in larger experimental colonies. In contrast, we found no significant associations between colony size and genetic diversity of key pathogen-recognition receptors, toll-like receptors (TLRs) and the Major Histocompatibility Complex (MHC) or genome-wide heterozygosity. We conclude that settlement decisions may be flexible within individuals and, thus, are likely to be primarily determined by the current immunological status, rather than fixed immunogenetic traits. Our study sheds new light on the complex interface between immunity and sociality in animals.

Colony size as a predictor of breeding behaviour in a common waterbird.

The choice of colony size may have profound consequences for individual fitness in colonially breeding birds, but at the same time it may require certain behavioural adaptations. Here, we aimed to examine behavioural divergence of common terns Sterna hirundo nesting in colonies of different size. For this purpose, we promoted establishment of small (<35 pairs) and large (>100 pairs) tern colonies under uniform ecological and environmental conditions by providing attractive patches of nesting substrate (floating rafts) at a single site. We combined video recording and GPS-tracking to assess communal and individual defence initiation rate, intra-specific aggression rate, and foraging flight characteristics. We found that birds from larger colonies more frequently engaged in communal defence and they performed longer foraging flights, while terns from smaller colonies more frequently showed individual defence behaviours. Also, intra-specific aggression rate was higher in smaller colonies, but this effect was primarily attributed to a higher proportion of edge breeding pairs, which were more aggressive. Our results suggest that various colony sizes may be associated with different behavioural syndromes, which comprise of diverse personality traits, such as social responsiveness, social tolerance, or propensity for aggression. It remains to be tested whether these behavioural differences reflect processes of phenotypic sorting among colonies of different size or whether they are a result of behavioural plasticity under different social contexts.