An enhancer of Agouti contributes to parallel evolution of cryptically colored beach mice.

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.

Two pup vocalization types are genetically and functionally separable in deer mice.

Vocalization is a widespread social behavior in vertebrates that can affect fitness in the wild. Although many vocal behaviors are highly conserved, heritable features of specific vocalization types can vary both within and between species, raising the questions of why and how some vocal behaviors evolve. Here, using new computational tools to automatically detect and cluster vocalizations into distinct acoustic categories, we compare pup isolation calls across neonatal development in eight taxa of deer mice (genus Peromyscus) and compare them with laboratory mice (C57BL6/J strain) and free-living, wild house mice (Mus musculus domesticus). Whereas both Peromyscus and Mus pups produce ultrasonic vocalizations (USVs), Peromyscus pups also produce a second call type with acoustic features, temporal rhythms, and developmental trajectories that are distinct from those of USVs. In deer mice, these lower frequency "cries" are predominantly emitted in postnatal days one through nine, whereas USVs are primarily made after day 9. Using playback assays, we show that cries result in a more rapid approach by Peromyscus mothers than USVs, suggesting a role for cries in eliciting parental care early in neonatal development. Using a genetic cross between two sister species of deer mice exhibiting large, innate differences in the acoustic structure of cries and USVs, we find that variation in vocalization rate, duration, and pitch displays different degrees of genetic dominance and that cry and USV features can be uncoupled in second-generation hybrids. Taken together, this work shows that vocal behavior can evolve quickly between closely related rodent species in which vocalization types, likely serving distinct functions in communication, are controlled by distinct genetic loci.

A chromosomal inversion contributes to divergence in multiple traits between deer mouse ecotypes.

How locally adapted ecotypes are established and maintained within a species is a long-standing question in evolutionary biology. Using forest and prairie ecotypes of deer mice (Peromyscus maniculatus), we characterized the genetic basis of variation in two defining traits-tail length and coat color-and discovered a 41-megabase chromosomal inversion linked to both. The inversion frequency is 90% in the dark, long-tailed forest ecotype; decreases across a habitat transition; and is absent from the light, short-tailed prairie ecotype. We implicate divergent selection in maintaining the inversion at frequencies observed in the wild, despite high levels of gene flow, and explore fitness benefits that arise from suppressed recombination within the inversion. We uncover a key role for a large, previously uncharacterized inversion in the evolution and maintenance of classic mammalian ecotypes.