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

Claire Armstrong,Helen Hipperson,Matt Clark,Gavin J Horsburgh,Lawrence Percival-Alwyn,Terry Burke,Clemens Küpper,David S Richardson,Lewis G Spurgin

doi:10.1002/evl3.38

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.

Highlights

Since the time of Darwin, evolutionary biologists have sought to understand how natural selection and random chance act to shape the extraordinary diversity we see in nature
Using RAD sequencing, we examined fine-scale population structure among Berthelot’s pipit populations, finding withinarchipelago genetic structuring between island populations, as well as confirming the previously detected patterns of amongarchipelago variation
After controlling for demographic history, we identified candidate SNPs associated with the ecologically important traits of bill length and malaria resistance

Summary

Introduction

Since the time of Darwin, evolutionary biologists have sought to understand how natural selection and random chance act to shape the extraordinary diversity we see in nature. GENES, BEAKS, AND DISEASE IN PIPITS whether these differences were the product of natural selection, or random processes that are the feature of evolutionary histories of small island populations. Our study shows that combining genetic techniques with ecological study is a powerful way to understand how natural selection acts in island populations. Phenotypic divergence between populations may be driven by natural selection acting upon adaptive traits, by genetic drift mediated by demographic forces, or by a combination of the two. Molecular markers have been used since the 1960s to characterize genetic diversity within and among populations (Lewontin and Hubby 1966; Kreitman 1983), identify demographic patterns (Jorde et al 1997; Garris et al 2005), and infer adaptation (Hughes and Nei 1988; Zhang et al 1998), and have been instrumental in the study of reproductive isolation and speciation

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