Balanced polymorphism underlies long-standing adaptation for seasonal camouflage in the least weasel

Unraveling how adaptive traits originate and evolve is key to understanding the mechanisms shaping species’ diversity and their adaptive potential. Seasonal color molts, from summer-brown to winter-white, evolved in at least 21 mammals and birds to maintain camouflage in environments with seasonal snow, but the occurrence of winter-brown morphs reflects seemingly convergent local adaptation to distinct snow conditions. In the least weasel (Mustela nivalis), alternative winter morphs map to the pigmentation gene MC1R, but the evolutionary history and functional basis of this variation remained unknown. Using in vitro cellular assays, we show that winter-brown coats are caused by a derived protein-coding amino acid substitution that reduces MC1R affinity to its ligands, ASIP and α-MSH. Using targeted enrichment and sequencing, we find that this mutation arose de novo within the species, around one million years ago, and was maintained across the geographically structured populations formed during its evolution in Europe. Using simulations, we show that genetic drift is unlikely to explain the long-term maintenance of this variant at intermediate frequencies, which can be driven by spatially varying selection, anchoring local adaptive responses. Our results underscore how long-standing adaptive variation can fuel recurrent adaptation to heterogeneous environments through time.