Genomic associations with bill length and disease reveal drift and selection across island bird populations

Abstract

Island species provide excellent models for investigating how selection and drift operate in wild populations, and for determining how these processes act to influence local adaptation and speciation. Here, we examine the role of selection and drift in shaping genomic and phenotypic variation across recently separated populations of Berthelot's pipit (Anthus berthelotii), a passerine bird endemic to three archipelagos in the Atlantic. We first characterized genetic diversity and population structuring that supported previous inferences of a history of recent colonizations and bottlenecks. We then tested for regions of the genome associated with the ecologically important traits of bill length and malaria infection, both of which vary substantially across populations in this species. We identified a SNP associated with variation in bill length among individuals, islands, and archipelagos; patterns of variation at this SNP suggest that both phenotypic and genotypic variation in bill length is largely shaped by founder effects. Malaria was associated with SNPs near/within genes involved in the immune response, but this relationship was not consistent among archipelagos, supporting the view that disease resistance is complex and rapidly evolving. Although we found little evidence for divergent selection at candidate loci for bill length and malaria resistance, genome scan analyses pointed to several genes related to immunity and metabolism as having important roles in divergence and adaptation. Our findings highlight the utility and challenges involved with combining association mapping and population genetic analysis in nonequilibrium populations, to disentangle the effects of drift and selection on shaping genotypes and phenotypes.

Adaptive landscape genetics and malaria across divergent island bird populations

“…We used previously identified candidate SNPs linked to malaria infection across populations (from a GWAS analysis performed on RAD‐seq SNPs; Armstrong et al, ) and TLR4 SNPs (González‐Quevedo et al, ) to investigate the relationship between potentially adaptive genetic variation and avian malaria within two island populations of Berthelot's pipits. In addition to testing for associations with infection status, we calculated the malaria risk at each sampling location, predicted by modeling fine‐scale environmental drivers of malaria infection.…”

“…Following the colonization of the Madeiran archipelago from the Canary Islands ca. 8,500 years ago (Spurgin, Illera, Jorgensen, Dawson, & Richardson, ; but see Valente et al, ), there has been a lack of gene flow between the archipelagos (Illera, Emerson, & Richardson, ; Spurgin et al, ), potentially facilitating local adaptation and divergent selection (Armstrong et al, ). Malaria infection shows high spatial variability in this species, both between and within islands, making it a highly suitable model for investigating the role of spatial scale in pathogen‐mediated selection.…”

“…Furthermore, evidence of positive selection at TLR4 in Berthelot's pipits suggests it may be an evolutionarily important locus (González‐Quevedo et al, ). In this study, we (a) test for associations between Plasmodium infection status (the only Haemosporidian genus commonly detected; >1% prevalence) in this species (Spurgin et al, ), and variation at TLR4 and two SNPs previously identified in a GWAS of malaria infection across Berthelot's pipit populations (Armstrong et al, ); (b) determine the environmental predictors of malaria risk on Porto Santo; (c) compare genetic associations with malaria risk in Porto Santo and Tenerife, utilizing the above measures of malaria risk for Porto Santo, and those previously calculated for Tenerife (González‐Quevedo et al, , ).…”

“…Following the colonization of the Madeiran archipelago from the Canary Islands ca. 8,500 years ago (Spurgin, Illera, Jorgensen, Dawson, & Richardson, 2014; but see Valente et al, 2017), there has been a lack of gene flow between the archipelagos (Illera, Emerson, & Richardson, 2007;Spurgin et al, 2014), potentially facilitating local adaptation and divergent selection (Armstrong et al, 2018).…”

The roles of geography, climate and sexual selection in driving divergence among insect populations on mountaintops

“…morphology and behaviour) variations among animal populations can result from natural selection (Schluter, 2001), and sexual selection is often decisive in the maintenance of differentiation via female choice (Panhuis, Butlin, Zuk, & Tregenza, 2001;Wells & Henry, 1998). Random processes, such as founder effects, drift and mutation, also promote phenotypic and genetic differentiation (Armstrong et al, 2018;Hoeck, Bollmer, Parker, & Keller, 2010;Irwin, Thimgan, & Irwin, 2008). The action of deterministic and stochastic forces becomes especially overt in populations of patchy or heterogeneous habitats, where adaptations to local conditions may be favoured by a reduction of gene flow or where reproduction and survival are more prone to undergo strong chance effects (Nosil, Egan, & Funk, 2008;Shafer & Wolf, 2013).…”