Targeted resequencing reveals a single origin of a beneficial pigment allele in young populations of beach mice

To understand how organisms adapt to novel habitats, which involves demographic and selective events, we require knowledge of the evolutionary history of both populations and selected alleles. There are still few cases in which the precise mutations (and hence defined alleles) that contribute to adaptive change have been identified in nature; one exception is the genetic basis of camouflaging pigmentation of oldfield mice (Peromyscus polionotus) that have colonized the sandy dunes of Florida’s Gulf Coast. To understand the genomic footprint of colonization, we first resequenced 5,000 1.5kb non-coding regions as well as a 160kb genomic region surrounding the melanocortin-1 receptor (Mc1r), a gene that contributes to pigmentation differences, in beach and mainland populations. Using a genome-wide phylogenetic approach, we recovered a single monophyletic group comprised of beach mice, consistent with a single colonization event of the Gulf Coast. We also found evidence of a severe founder event, estimated to have occurred less than 3,000 years ago, followed by subsequent migration between mainland and beach populations. In this demographic context, we found a single origin of the derived light Mc1r allele and evidence in patterns of nucleotide variation consistent with positive selection. Together, these data allow us to reconstruct and compare the evolutionary history of populations and alleles to better understand how adaptive evolution following the colonization of a novel habitat proceeds in nature.