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

Abstract

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.

Fig. 1. Study area.

Location of black-headed gull populations sampled in this study.

Fig. 2. Genetic population differentiation.

Pairwise D_est between seven black-headed gull populations were estimated for different immune genes (amino acid variants) and neutral microsatellite markers. D_est values were block-centred for each pairwise comparison across all the markers. Median (central line), Q1 and Q3 quantiles (box) and outlier range (whiskers) are shown for each marker.

Fig. 3. Population differentiation at the MHC-II.

Discriminant functions (DF1 and DF2) were calculated with the discriminant analysis of principal components (DAPC) for the MHC-II (amino acid variants) across seven black-headed gull populations (each population marked with a different colour). The reassignment of individuals into their prior groups (populations) is shown below the DAPC scatterplot. Each bar represents proportional posterior membership probability of each individual into each population.

Fig. 4. Selection on MHC genes.

Sites under pervasive and episodic diversifying (positive) selection are marked above the dS-dN curve with filled and open dots, respectively. Sites under purifying (negative) selection are marked below the dS-dN curve with open squares. Human peptide-binding region (PBR) sites (according to Saper et al. for MHC-I and Brown et al. for MHC-II) are marked in light green, sites previously identified as under positive selection in non-passerine birds (according to Minias et al. 2018) are marked in light blue, while overlapping sites (human PBR sites under positive selection in non-passerines) are marked in dark blue.