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Convergent Evolution of Seasonal Camouflage in Response to Reduced Snow Cover Across the Snowshoe Hare Range

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Convergent Evolution of Seasonal Camouflage in Response to Reduced Snow Cover Across the Snowshoe Hare Range ORIGINAL ARTICLE doi:10.1111/evo.13976 Convergent evolution of seasonal camouflage in response to reduced snow cover across the snowshoe hare range Matthew R. Jones,1,2 L. Scott Mills,3,4 Jeffrey D. Jensen,5 and Jeffrey M. Good1,3,6 1Division of Biological Sciences, University of Montana, Missoula, Montana 59812 2E-mail: [email protected] 3Wildlife Biology Program, University of Montana, Missoula, Montana 59812 4Office of Research and Creative Scholarship, University of Montana, Missoula, Montana 59812 5School of Life Sciences, Arizona State University, Tempe, Arizona 85281 6E-mail: [email protected] Received January 22, 2020 Accepted April 2, 2020 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 in re- sponse to climate change. We used extensive range-wide genomic data to (1) resolve broad patterns of population structure and gene flow and (2) investigate the factors shaping the origins and distribution of winter-brown camouflage variation. Incoastal Pacific Northwest (PNW) populations, winter-brown camouflage is known to be determined by a recessive haplotype atthe Agouti pigmentation gene. Our phylogeographic analyses revealed deep structure and limited gene flow between PNW and more north- ern 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 of this population fur- ther show that this masking effect would greatly slow the selective increase of the winter-brown Agouti allele should it suddenly become beneficial (e.g., owing to dramatic declines in snow cover). Our findings underscore how allelic dominance canshapethe geographic extent and rate of convergent adaptation in response to rapidly changing environments. KEY WORDS: Climate change, dominance, introgression, local adaptation, migration, parallel evolution. In response to a shared selection pressure, populations may spread quickly (Fisher 1937) and potentially allow for rapid adapt through the migration of beneficial alleles or through adaptive responses to changing environments (Bay et al. 2017). independent mutations that result in the evolution of convergent However, the spread of adaptive variation may be limited at phenotypes (Wright 1931; Haldane 1932; and see Ralph and broad geographic scales, and populations may have to rely on in- Coop 2015). Distinguishing between these scenarios is cru- dependent standing genetic variation or new mutations to evolve cial to understand the capacity of populations to adapt rapidly convergent traits (i.e., “convergent evolution” following Arendt to environmental change (Bridle and Vines 2007; Hoffmann and Reznick [2008]). Although there is considerable evidence for and Sgrò 2011; Ralph and Coop 2015). If gene flow between both adaptation through gene flow and independent mutations populations is sufficiently high, then beneficial variation may in nature (Hoekstra and Nachman 2003; Hoekstra et al. 2005; © 2020 The Authors. Evolution © 2020 The Society for the Study of Evolution. 1 Evolution M. R. JONES ET AL. Steiner et al. 2008; Rosenblum et al. 2010; Dobler et al. 2012; atively high amounts of gene flow, genetic dominance may have Marques et al. 2017; Kreiner et al. 2019), few empirical studies little to no effect on the probability of adaptation via migration have examined the specific factors that influence these outcomes versus de novo mutation. In fact, the masking of low frequency in natural populations (Ralph and Coop 2015). recessive alleles may result in weaker purifying selection in in- When a species range encompasses a mosaic of habitats, the tervening habitats and therefore facilitate the spread of adaptive relative probability of adaptation through gene flow versus inde- variation through gene flow (Ralph and Coop 2015), although pendent mutation is predicted to be primarily a function of the this hypothesis remains to be tested. distance between habitat patches (in units of dispersal distance) Snowshoe hares (Lepus americanus) are one of at least 21 and the strength of selection against locally adaptive alleles in in- species that have evolved seasonal molts to white winter coats tervening habitats (Slatkin 1973; Ralph and Coop 2010, 2015). In to maintain camouflage in snowy winter environments. Because general, as distance between patches and the strength of purify- color molts are cued by photoperiod, and hence may become ing selection in intervening habitats increases, so does the relative mismatched under rapidly changing environments (Mills et al. probability of adaptation through independent mutations. Adap- 2013; Zimova et al. 2018), seasonal camouflage provides a use- tation via independent mutations is therefore predicted to be more ful trait to understand adaptation to climate change (Mills et al. common in widespread populations where dispersal distance is 2013, 2018; Zimova et al. 2016, 2018; Jones et al. 2018). Re- short relative to the total range size (Ralph and Coop 2010). For duction in the extent and duration of snow cover is one of the example, rock pocket mice (Chaetodipus intermedius)havere- strongest signatures of climate change in the Northern hemi- peatedly evolved melanistic coats across patchy lava flows in sphere (Knowles et al. 2006; Brown and Mote 2009), suggest- the southwestern United States. Although substantial gene flow ing that selection should increasingly favor delayed winter-white between adjacent lava flows has likely resulted in the migration molts in snowshoe hares to reduce the total duration of coat color of melanic alleles (Hoekstra et al. 2005), melanism is attributed mismatch. However, below some annual snow cover threshold, to different mutations across disparate lava flows (Hoekstra and populations are predicted to maintain brown coloration during the Nachman 2003; Nachman et al. 2003; Harris et al. 2020). Theo- winter (Mills et al. 2018). Consistent with this, snowshoe hares retical models further predict that the relative probability of adap- maintain brown winter camouflage in some temperate environ- tation via independent mutations increases rapidly with distance ments with reduced snow cover (Nagorsen 1983), a strategy that between lava flows (over the scale of tens to hundreds of kilo- should be increasingly favored under climate change (Jones et al. meters; Ralph and Coop 2015), due in large part to strong selec- 2018; Mills et al. 2018). tion against coat color mismatch (Hoekstra et al. 2004; Pfeifer Winter-brown snowshoe hares are common in coastal re- et al. 2018; Barrett et al. 2019). Thus, there is a clear trade-off gions of the Pacific Northwest (PNW), where this Mendelian between dispersal distance and the strength of purifying selec- trait is determined by a recessive variant of the Agouti pigmen- tion that strongly dictates the probability of adaptation through tation gene (Jones et al. 2018). The locally adaptive Agouti vari- convergent evolution or gene flow. ant was introduced into snowshoe hares by hybridization with The effect of genetic dominance on the probability of con- black-tailed jackrabbits nearly 7000–14,000 generations ago and vergent evolution has not yet been thoroughly explored (Ralph subsequently experienced a local selective sweep within the last and Coop 2015). “Haldane’s sieve” (Turner 1981) predicts that few thousand generations (Jones et al. 2020). Occasional records de novo dominant mutations enjoy a much greater probability of winter-brown camouflage also occur in more northern regions of fixation compared to de novo recessive mutations (probabil- along the Pacific coast (e.g., Canada and Alaska) and in east- ity of fixation ≈ 2hs,whereh = dominance coefficient and s ern North America (Gigliotti et al. 2017; Mills et al. 2018). = selection coefficient), because rare dominant mutations are Although hares are expected to be more or less continuously visible to selection (Haldane 1924). As de novo beneficial re- distributed along suitable Pacific coast environments, there is a cessive mutations are masked to selection when rare, those that deep split and little evidence of recent gene flow between the do ultimately reach fixation may spend a longer period of time northern “Boreal” populations and southern “PNW” populations drifting at low frequency (Teshima and Przeworski 2006). Like- (Cheng et al. 2014; Melo-Ferreira et al. 2014). Given this his- wise, rare recessive migrant alleles are expected to exhibit the toric population structure, it remains unclear whether the dis- same behavior, which may allow more time for mutation to gen- tribution of winter-brown camouflage across populations from erate “competing” convergent phenotypes upon which selection disparate parts of the range reflects independent genetic origins can act. However, Orr and Betancourt (2001) demonstrated that (i.e., trait convergence) or spread of the introgressed PNW Agouti genetic dominance has no effect on the probability of fixation allele. for alleles in mutation-selection balance because recessive alleles Here, we use new and previously published genetic data have a higher mutation-selection balance frequency. Thus, for rel- to investigate the roles of gene flow and mutation in shaping 2 EVOLUTION 2020 CONVERGENT EVOLUTION OF SEASONAL CAMOUFLAGE A 1 P(winter-white) 0 AK2 AK1 NT YT BC3 SK BC2 BC1 33.8 ME MN PA WA B (26.9-42.3) BC2 NY 1.0 NS MT NY OR WY ME NS MI YT PA 97.2 SK CO (77.4-120.8) NT UT BC3 AK1 AK2 CO UT 47.1 WY (37.2-58.2) C Rockies Boreal 1.0 18.8 MT PNW (14.4-22.7) 1.0 BC WA ancestry OR proportion OR WA BC1 MT Figure 1. (A) Range-wide phylogeography of snowshoe hares based on whole exome sequences.
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