The origin and spread of locally adaptive seasonal camouflage in snowshoe hares

Adaptation is central to population persistence in the face of environmental change, yet we seldom precisely understand the origin and spread of adaptive variation in natural populations. Snowshoe hares (Lepus americanus) along the Pacific Northwest (PNW) coast have evolved brown winter camouflage through positive selection on recessive variation at the Agouti pigmentation gene introgressed from black-tailed jackrabbits (L. californicus). Here we combine new and published whole genome and exome sequences with targeted genotyping of Agouti in order to investigate the evolutionary history of local seasonal camouflage adaptation in the PNW. We find evidence of significantly elevated inbreeding and mutational load in coastal winter-brown hares, consistent with a recent range expansion into temperate coastal environments that incurred indirect fitness costs. The genome-wide distribution of introgression tract lengths supports a pulse of hybridization near the end of the last glacial maximum, which may have facilitated range expansion via introgression of winter-brown camouflage variation. However, signatures of a selective sweep at Agouti indicate a much more recent spread of winter-brown camouflage. Through simulations we show that the delay between the hybrid origin and subsequent selective sweep of the recessive winter-brown allele can be largely attributed to the limits of natural selection imposed by simple allelic dominance. We argue that while hybridization during periods of environmental change may provide a critical reservoir of adaptive variation at range edges, the probability and pace of local adaptation will strongly depend on population demography and the genetic architecture of introgressed variation.