Genomic associations with poxvirus across divergent island populations in Berthelot's pipit

Abstract

Understanding the mechanisms and genes that enable animal populations to adapt to pathogens is important from an evolutionary, health and conservation perspective. Berthelot's pipit (Anthus berthelotii) experiences extensive and consistent spatial heterogeneity in avian pox infection pressure across its range of island populations, thus providing an excellent system with which to examine how pathogen-mediated selection drives spatial variation in immunogenetic diversity. Here, we test for evidence of genetic variation associated with avian pox at both an individual and population-level. At the individual level, we find no evidence that variation in MHC class I and TLR4 (both known to be important in recognising viral infection) was associated with pox infection within two separate populations. However, using genotype-environment association (Bayenv) in conjunction with genome-wide (ddRAD-seq) data, we detected strong associations between population-level avian pox prevalence and allele frequencies of single nucleotide polymorphisms (SNPs) at a number of sites across the genome. These sites were located within genes involved in cellular stress signalling and immune responses, many of which have previously been associated with responses to viral infection in humans and other animals. Consequently, our analyses indicate that pathogen-mediated selection may play a role in shaping genomic variation among relatively recently colonised island bird populations and highlight the utility of genotype-environment associations for identifying candidate genes potentially involved in host-pathogen interactions.

Keywords: adaptation; avian pox virus; birds; genotype-environment association; pathogen-mediated selection.

FIGURE 1

Map of the 12 islands sampled for Berthelot's pipits across its Macaronesian range. Populations are coloured according to their overall estimated pox prevalence across the 15‐year sampling period. M, Madeira; PS, Porto Santo; DG, Deserta Grande; SG, Selvagem Grande; LP, La Palma; EH, El Hierro; GOM, La Gomera; TF, Tenerife; GC, Gran Canaria; FV, Fuerteventura; GRA, La Graciosa; LZ, Lanzarote

FIGURE 2

Prevalence of pox infection among Berthelot's pipits with and without malaria infection on Porto Santo and Tenerife. Numbers above the bars represent sample sizes

FIGURE 3

Bayes factor values versus absolute Spearman's rank correlation coefficients (ρ), averaged from five replicate runs, for genome‐wide ddRAD SNPs among 13 Berthelot's pipit populations. SNPs were considered candidates for adaptation to population‐level pox prevalence by Bayenv2.0 if they ranked in the highest 1% of Bayes factor values (≥7.4, threshold indicated by the vertical red line) and 10% of Spearman's ρ (threshold indicated by the horizontal red line). Fourteen SNPs were identified as candidates (those in red)

FIGURE 4

Minor allele frequency (MAF) distribution patterns of 14 candidate SNPs associated with population‐level pox prevalence identified by Bayenv2.0 across populations of Berthelot's pipit. Nearby genes are noted below the SNP names. Populations are first grouped by archipelago (CI, Canary Islands; M, Madeira; S, Selvagens) and then ordered according to population‐level pox prevalence (highest‐lowest). Pox‐free populations are indicated by an asterisk. FV, Fuerteventura; LZ, Lanzarote; GC, Gran Canaria; TF, Tenerife; GOM, La Gomera; TEID, Teide; GRA, La Graciosa; LP, La Palma; EH, El Hierro; PS, Porto Santo; DG, Deserta Grande; M, Madeira; SG, Selvagem Grande