期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：27
DOI：10.1073/pnas.2202862119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
Oldfield mice have independently colonized the white-sand beaches of Florida’s Gulf and Atlantic coasts, where they have evolved light fur that camouflages them from visually hunting predators. We find that fur color is strongly associated with DNA variation in a small regulatory region of the
Agouti signaling protein, which contains an enhancer that drives expression in mouse skin. This regulatory allele is found in all light-colored beach mice on both coasts, despite being separated by >1,000 km. Based on patterns of DNA variation within and between populations, our results suggest that this
Agouti allele arose in the mainland and then, has spread to and been selected in two independent beach mouse lineages, thereby facilitating their rapid and parallel evolution.
Identifying the genetic basis of repeatedly evolved traits provides a way to reconstruct their evolutionary history and ultimately investigate the predictability of evolution. Here, we focus on the oldfield mouse (
Peromyscus polionotus), which occurs in the southeastern United States, where it exhibits considerable color variation. Dorsal coats range from dark brown in mainland mice to near white in mice inhabiting sandy beaches; this light pelage has evolved independently on Florida’s Gulf and Atlantic coasts as camouflage from predators. To facilitate genomic analyses, we first generated a chromosome-level genome assembly of
Peromyscus polionotus subgriseus. Next, in a uniquely variable mainland population (
Peromyscus polionotus albifrons), we scored 23 pigment traits and performed targeted resequencing in 168 mice. We find that pigment variation is strongly associated with an ∼2-kb region ∼5 kb upstream of the
Agouti signaling protein coding region. Using a reporter-gene assay, we demonstrate that this regulatory region contains an enhancer that drives expression in the dermis of mouse embryos during the establishment of pigment prepatterns. Moreover, extended tracts of homozygosity in this
Agouti region indicate that the light allele experienced recent and strong positive selection. Notably, this same light allele appears fixed in both Gulf and Atlantic coast beach mice, despite these populations being separated by >1,000 km. Together, our results suggest that this identified
Agouti enhancer allele has been maintained in mainland populations as standing genetic variation and from there, has spread to and been selected in two independent beach mouse lineages, thereby facilitating their rapid and parallel evolution.
