Genetic variation at innate and adaptive immune genes - contrasting patterns of differentiation and local adaptation in a wild gull.

Immunogenetic variation in natural vertebrate populations is expected to respond to spatial and temporal fluctuations in pathogen assemblages. While spatial heterogeneity in pathogen-driven selection enhances local immunogenetic adaptations and population divergence, different immune genes may yield contrasting responses to the environment. Here, we investigated population differentiation at the key pathogen recognition genes of the innate and adaptive immune system in a colonial bird species, the black-headed gull Chroicocephalus ridibundus. We assessed genetic variation at three toll-like receptor (TLR) genes (innate immunity) and the major histocompatibility complex (MHC) class I and II genes (adaptive immunity) in gulls from seven colonies scattered across Poland. As expected, we found much greater polymorphism at the MHC than TLRs. Population differentiation at the MHC class II, but not MHC-I, was significantly stronger than at neutral microsatellite loci, suggesting local adaptation. This could reflect spatial variation in the composition of extracellular parasite communities (e.g., helminths), possibly driven by sharp differences in habitat structure between colonies. Despite contrasting patterns of population differentiation, both MHC classes showed similar regimes of diversifying selection. Some significant population differentiation was also observed at TLRs, suggesting that innate immune receptors may respond to fine-scale spatial variation in pathogen pressure, although this pattern could have been enhanced by drift. Our results suggested that local adaptation at the pathogen recognition immune genes can be maintained at relatively small or moderate spatial scales in species with high dispersal potential and they highlighted the complexity of immunogenetic responses of animals to heterogeneous environments.

Contrasting haemoparasite prevalence in larid species with divergent ecological niches and migration patterns.

Haemoparasites represent a diverse group of vector-borne parasites that infect a wide range of vertebrate hosts. In birds, haemoparasite infection rates may be associated with various ecological and life history traits, including habitat choice, colony size and migration distance. Here, we molecularly assessed the prevalence of 3 main haemoparasite genera (Plasmodium, Haemoproteus and Leucocytozoon) in 2 bird species with different habitat preferences and migratory behaviour: black-headed gulls (Chroicocephalus ridibundus) and common terns (Sterna hirundo). We found that gulls showed a much higher prevalence and diversity of Plasmodium or Haemoproteus (ca. 60% of individuals infected) than terns (zero prevalence). The prevalence of Leucocytozoon was low in both species (<3%). The differences in haemoparasite prevalences may be primarily driven by varying vector encounter rate resulting from different habitat preferences, as black-headed gulls mainly use vector-rich vegetated freshwater habitats, whereas common terns often use vector-poor coastal and brackish habitats. Since common terns migrate further than black-headed gulls, our results did not provide support for an association between haemoparasite prevalence and migratory distance. In gulls, we found a negative association between colony size and infection rates, suggestive of an ideal despotic distribution, and phylogenetic analyses of detected haemoparasite lineages provided evidence for higher host specificity in Haemoproteus than Plasmodium. Our results suggest that the preference for coastal areas and less vegetated habitats in terns may reduce haemoparasite infection rates compared to other larids, regardless of their migratory distance, emphasizing the role of ecological niches in parasite exposure.

Relaxation of selective constraints shapes variation of toll-like receptors in a colonial waterbird, the black-headed gull.

Nonspecific innate immune response is activated by toll-like receptors (TLRs), which recognize conserved molecular motifs characteristic for a broad spectrum of pathogens. In this study, we examined nucleotide substitution patterns and allelic diversity at five TLR genes in a wild nonpasserine bird, the black-headed gull Chroicocephalus ridibundus. We hypothesized that balancing selection can maintain high allelic diversity of TLR genes in the black-headed gull because of its ecological characteristics, coloniality, and migratoriness, which are associated with increased exposure and transmission of pathogens. Although we found moderately high levels of sequence polymorphism (8-49 haplotypes retrieved per locus within a sample of 60 individuals), most of these haplotypes were recorded at low frequencies within our study population. At the same time, we found no convincing evidence for the role of balancing selection in the maintenance of this variation (Tajima's D < 0.5), and sites with a significant excess of nonsynonymous mutations (dN/dS > 1) were recorded only at two loci (TLR5 and TLR7). This pattern is consistent with relaxation of selective constraints, where most mutations are slightly deleterious and usually removed by purifying selection. No differences in the diversity and nucleotide substitution rates were found between endosomal loci responsible for viral RNA sensing and loci responsible for the recognition of extracellular pathogens. Our study provides the first information on evolutionary mechanisms shaping polymorphism of TLRs in a species from Lari suborder (gulls and allies) and suggests that TLR genes may be poorly responsive to ecological and life-history characteristics of hosts.

Plumage quality mediates a life-history trade-off in a migratory bird.

BACKGROUND: Moult is one of the most costly activities in the annual cycle of birds and most avian species separate moult from other energy-demanding activities, such as migration. To this end, young birds tend to undergo the first post-juvenile moult before the onset of migration, but in some species the time window for the pre-migratory feather replacement is too narrow. We hypothesized that in such species an increased investment in the structural quality of juvenile feathers may allow to retain juvenile plumage throughout the entire migratory period and delay moult until arriving at wintering grounds, thus avoiding a moult-migration overlap. METHODS: The effect of juvenile plumage quality on the occurrence of moult-migration overlap was studied in a migratory shorebird, the common snipe Gallinago gallinago. Ca. 400 of first-year common snipe were captured during their final stage of autumn migration through Central Europe. The quality of juvenile feathers was assessed as the mass-length residuals of retained juvenile rectrices. Condition of migrating birds was assessed with the mass of accumulated fat reserves and whole-blood hemoglobin concentration. Path analysis was used to disentangle complex interrelationships between plumage quality, moult and body condition. RESULTS: Snipe which grew higher-quality feathers in the pre-fledging period were less likely to initiate moult during migration. Individuals moulting during migration had lower fat loads and hemoglobin concentrations compared to non-moulting birds, suggesting a trade-off in resource allocation, where energetic costs of moult reduced both energy reserves available for migration and resources available for maintenance of high oxygen capacity of blood. CONCLUSIONS: The results of this study indicate that a major life-history trade-off in a migratory bird may be mediated by the quality of juvenile plumage. This is consistent with a silver spoon effect, where early-life investment in feather quality affects future performance of birds during migration period. Our results strongly suggest that the juvenile plumage, although retained for a relatively short period of time, may have profound consequences for individuals' fitness.

Longevity is associated with relative brain size in birds.

Brain size of vertebrates has long been recognized to evolve in close association with basic life-history traits, including lifespan. According to the cognitive buffer hypothesis, large brains facilitate the construction of behavioral responses against novel socioecological challenges through general cognitive processes, which should reduce mortality and increase lifespan. While the occurrence of brain size-lifespan correlation has been well documented in mammals, much less evidence exists for a robust link between brain size and longevity in birds. The aim of this study was to use phylogenetically controlled comparative approach to test for the relationship between brain size and longevity among 384 avian species from 23 orders. We used maximum lifespan and maximum reproductive lifespan as the measures of longevity and accounted for a set of possible confounding effects, such as allometry, sampling effort, geographic patterns, and life-history components (clutch size, incubation length, and mode of development). We found that both measures of longevity positively correlated with relative (residual) brain size. We also showed that major diversification of brain size preceded diversification of longevity in avian evolution. In contrast to previous findings, the effect of brain size on longevity was consistent across lineages with different development patterns, although the relatively low strength of this correlation could likely be attributed to the ubiquity of allomaternal care associated with the altricial mode of development. Our study indicates that the positive relationship between brain size and longevity in birds may be more general than previously thought.

When moult overlaps migration: moult-related changes in plasma biochemistry of migrating common snipe.

Moult of feathers entails considerable physiological and energetic costs to an avian organism. Even under favourable feeding conditions, endogenous body stores and energy reserves of moulting birds are usually severely depleted. Thus, most species of birds separate moult from other energy-demanding activities, such as migration or reproduction. Common snipe Gallinago gallinago is an exception, as during the first autumn migration many young snipe initiate the post-juvenile moult, which includes replacement of body feathers, lesser and median wing coverts, tertials, and rectrices. Here, we evaluated moult-related changes in blood plasma biochemistry of the common snipe during a period of serious trade-off in energy allocation between moult and migration. For this purpose, concentrations of basic metabolites in plasma were evaluated in more than 500 young snipe migrating through Central Europe. We found significant changes in the plasma concentrations of total protein, triglyceride and glucose over the course of moult, while the concentrations of uric acid and albumin did not change. Total protein concentration increased significantly in the initial stage of moult, probably as a result of increased production of keratin, but it decreased to the pre-moult level at the advanced stage of moult. Plasma triglyceride concentration decreased during the period of tertial and rectrice moult, which reflected depletion of endogenous fat reserves. By contrast, glucose concentration increased steadily during the course of moult, which could be caused by increased catabolism of triglycerides (via gluconeogenesis) or, alternatively, due to increased glucocorticoids as a stress response. Our results suggest that physiological changes associated with moult may be considered important determinants of the low pace of migration typical of the common snipe.