Biology subjects

Mills, L. S.

Publications and source records attributed to Mills, L. S..

5 recordsLinked to original sources

bioRxiv2025

Museum genomics links MC1R alleles to adaptive winter coat color polymorphism in the long-tailed weasel

Understanding the architecture of biological adaptations is a major endeavor of evolutionary biology. Using Natural History collections, we study the genetic basis and evolution of white/brown winter coat color variation in the long-tailed weasel (Neogale frenata), a crucial phenological adaptation for camouflage in habitats with seasonal snow. We produced whole-genome sequencing data for museum specimens, along two winter color morph transition areas in North America, at the West and East coasts. Genome-wide association scans identified a single genomic region linked to color variation polymorphism with approximately 300kb and 200kb in the West and East regions, respectively, which included the pigmentation gene MC1R. We identified three MC1R alleles, two of which with deletions of nine or eight amino acids, alternatively associated with the winter brown morphs in the West and East, respectively. These deletions affect the second transmembrane domain, and in one case also the first extracellular loop, which in silico analyses predicted to impact the proteins function. Our findings show alternative intraspecific evolutionary solutions for environmental adaptation in long-tailed weasels, building on the evidence that major genes of the melanin production pathway are hotspots for recurrent and independent evolution of winter camouflage adaptation.

evolutionary biology↗

bioRxiv2025

Ancient 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 remain 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 -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 generated during its evolution in Europe. Using simulations, we show that genetic drift cannot explain the long-term maintenance of this variant, which is likely driven by spatially varying selection acting on the phenotypic polymorphism, anchoring local adaptive responses. Our results underscore how long-standing adaptive variation can fuel recurrent adaptation to heterogeneous environments through time.

evolutionary biology↗

bioRxiv2020

The legacy of recurrent introgression during the radiation of hares

AO_SCPLOWBSTRACTC_SCPLOWHybridization may often be an important source of adaptive variation, but the extent and long-term impacts of introgression have seldom been evaluated in the phylogenetic context of a radiation. Hares (Lepus) represent a widespread mammalian radiation of 32 extant species characterized by striking ecological adaptations and recurrent admixture. To understand the relevance of introgressive hybridization during the diversification of Lepus, we analyzed whole exome sequences (61.7 Mb) from 15 species of hares (1- 4 individuals per species), spanning the global distribution of the genus, and two outgroups. We used a coalescent framework to infer species relationships and divergence times, despite extensive genealogical discordance. We found high levels of allele sharing among species and show that this reflects extensive incomplete lineage sorting and temporally layered hybridization. Our results revealed recurrent introgression at all stages along the Lepus radiation, including recent gene flow between extant species since the last glacial maximum, but also pervasive ancient introgression occurring since near the origin of the hare lineages. We show that ancient hybridization between northern hemisphere species has resulted in shared variation of potential adaptive relevance to highly seasonal environments, including genes involved in circadian rhythm regulation, pigmentation, and thermoregulation. Our results illustrate how the genetic legacy of ancestral hybridization may persist across a radiation, leaving a long-lasting signature of shared genetic variation that may contribute to adaptation within and among species.

evolutionary biology↗

bioRxiv2019

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.

evolutionary biology↗

bioRxiv2019

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 rarely 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 temporal lag 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.

evolutionary biology↗