Convergent evolution of seasonal camouflage in response to reduced snow cover across the snowshoe hare range
Determining how different populations adapt to similar environments is fundamental to understanding the limits of adaptation under changing environments. Snowshoe hares (Lepus americanus) typically molt into white winter coats to remain camouflaged against snow. In some warmer climates, hares have evolved brown winter camouflage - an adaptation that may spread under climate change. We used extensive range-wide genomic data to 1) resolve broad-scale patterns of population structure and gene flow and 2) investigate the factors shaping the origins and distribution of winter-brown camouflage variation. In coastal Pacific Northwest (PNW) populations, winter-brown camouflage is known to be determined by a recessive haplotype at the Agouti pigmentation gene. Our phylogeographic analyses revealed deep structure and limited gene flow between PNW and more northern Boreal populations, where winter-brown camouflage is rare along the range edge. Genome sequencing of a winter-brown snowshoe hare from Alaska shows that it lacks the winter-brown PNW haplotype, reflecting a history of convergent phenotypic evolution. However, the PNW haplotype does occur at low frequency in a winter-white population from Montana, consistent with the spread of a locally deleterious recessive variant that is masked from selection when rare. Simulations show that if annual snow cover dramatically declined in the same population, then the predicted selective increase in frequency of the now beneficial winter-brown Agouti allele is likely to be extremely slow due to the same masking effect. Our findings underscore how allelic dominance can shape the geographic extent and rate of convergent adaptation in response to rapidly changing environments.