Genetic, phenotypic, and environmental drivers of local adaptation and climate change–induced maladaptation in a migratory songbird

Abstract

Understanding processes driving local adaptation in wild species is a key goal in evolutionary biology, but linking genotype to phenotype to environmental drivers of natural selection remains challenging. Even more rare are empirical examples of what happens when genotype and phenotype fail to keep pace with environmental change. Here, we explore these connections by conducting an integrative study on the breeding range of the yellow warbler ( Setophaga petechia ). Using genome-wide association studies (GWAS), we first identify loci associated with variation in bill morphology and individual quality. We then employ gene–environment association (GEA) analyses and find that precipitation is a key environmental driver of putative selection on bill shape. Finally, we test whether contemporary individuals whose bill shapes deviate from the historical relationship with precipitation experience increased stress (measured by telomere length) as a result of maladaptation. We also use historical DNA to test whether local populations have shifted their ranges over the past century, confirming that the observed changes are not due to range shifts. Our results align with predictions from GWAS and GEA analyses, indicating that birds with shallower bills in increasingly arid regions suffer higher stress (i.e., shorter telomeres) because of maladaptation. Overall, this study links genetic, phenotypic, and environmental data with stress biomarkers to improve understanding of the process of local adaptation and the consequence of failing to keep pace with changing climate conditions.