‘Haldane’s sieve’ predicts that de novo dominant mutations enjoy a much greater probability of fixation compared to de novo recessive mutations (probability of fixation ≈2 hs), because rare dominant mutations are visible to selection. The effect of genetic dominance on the probability of convergent evolution has not yet been thoroughly explored. Thus, there is a clear tradeoff between dispersal distance and the strength of purifying selection that strongly dictates the probability of adaptation through convergent evolution or gene flow. Theoretical models further predict that the relative probability of adaptation via independent mutations increases rapidly with distance between lava flows (over the scale of tens to hundreds of kilometers), due in large part to strong selection against coat color mismatch. Although substantial gene flow between adjacent lava flows has likely resulted in the migration of melanic alleles, melanism is attributed to different mutations across disparate lava flows. For example, rock pocket mice ( Chaetodipus intermedius) have repeatedly evolved melanistic coats across patchy lava flows in the southwestern United States.

Adaptation via independent mutations is therefore predicted to be more common in widespread populations where dispersal distance is short relative to the total range size. In general, as distance between patches and the strength of purifying selection in intervening habitats increases, so does the relative probability of adaptation through independent mutations. When a species range encompasses a mosaic of habitats, the relative probability of adaptation through gene flow versus independent mutation is predicted to be primarily a function of the distance between habitat patches (in units of dispersal distance) and the strength of selection against locally adaptive alleles in intervening habitats. While there is considerable evidence for both adaptation through gene flow and independent mutations in nature, few empirical studies have examined the specific factors that influence these outcomes in natural populations. However, the spread of adaptive variation may be limited at broad geographic scales, and populations may have to rely on independent standing genetic variation or new mutations to evolve convergent traits. If gene flow between populations is sufficiently high, then beneficial variation may spread quickly and potentially allow for rapid adaptive responses to changing environments. Distinguishing between these scenarios is crucial to understand the capacity of populations to adapt rapidly to environmental change. In response to a shared selection pressure, populations may adapt through the migration of beneficial alleles or through independent mutations that result in the evolution of convergent phenotypes. Our findings underscore how allelic dominance can shape the geographic extent and rate of convergent adaptation in response to rapidly changing environments. 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. 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. 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. 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. In coastal Pacific Northwest (PNW) populations, winter-brown camouflage is known to be determined by a recessive haplotype at the Agouti pigmentation gene.

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 some warmer climates, hares have evolved brown winter camouflage – an adaptation that may spread under climate change. Snowshoe hares ( Lepus americanus) typically molt into white winter coats to remain camouflaged against snow. Determining how different populations adapt to similar environments is fundamental to understanding the limits of adaptation under changing environments.

Rock pocket mouse genetics lab