Comparative Phylogeography Highlights the Double-Edged Sword of Climate Change Faced by Arctic- and Alpine-Adapted Mammals

March Comparative Phylogeography Highlights the Double-Edged Sword of Climate Change Faced by Arctic- and Alpine-Adapted Mammals Hayley C. Lanier 0 1 2 Aren M. Gunderson 0 1 2 Marcelo Weksler 0 1 2 Vadim B. Fedorov 0 1 2 Link E. Olson 0 1 2 0 a Current address: Department of Zoology & Physiology, University of Wyoming at Casper, Casper, Wyoming 82601, United States of America b Current address: Laboratorio de Ecoepidemiologia da Doenca de Chagas, Instituto Oswaldo Cruz , FIOCRUZ, Rio de Janeiro, RJ 21040-900 , Brazil 1 1 University of Alaska Museum, University of Alaska Fairbanks, Fairbanks, Alaska 99775, United States of America, 2 Institute of Arctic Biology, University of Alaska Fairbanks , Fairbanks, Alaska 99775 , United States of America 2 Funding: This work was supported by the following sources of funding: Alaska Department of Fish and Game (http://www.adfg.alaska.gov) State Wildlife Grant (Grant T-1-6) to LEO; National Science Foundation (http://www.nsf.gov) Doctoral Dissertation Improvement Grant (DEB-0808619) to LEO and HCL; Alaska EPSCoR (http://www.alaska.edu/epscor/) Dissertation Enhancement Grant (NSF EPS- 0092040, 0346770) to HCL; American Society of Mammalogists (http://www.mammalsociety.org) Grant in Aid of Research to HCL; and Alaska Quaternary Recent studies suggest that alpine and arctic organisms may have distinctly different phylogeographic histories from temperate or tropical taxa, with recent range contraction into interglacial refugia as opposed to post-glacial expansion out of refugia. We use a combination of phylogeographic inference, demographic reconstructions, and hierarchical Approximate Bayesian Computation to test for phylodemographic concordance among five species of alpine-adapted small mammals in eastern Beringia. These species (Collared Pikas, Hoary Marmots, Brown Lemmings, Arctic Ground Squirrels, and Singing Voles) vary in specificity to alpine and boreal-tundra habitat but share commonalities (e.g., cold tolerance and nunatak survival) that might result in concordant responses to Pleistocene glaciations. All five species contain a similar phylogeographic disjunction separating eastern and Beringian lineages, which we show to be the result of simultaneous divergence. Genetic diversity is similar within each haplogroup for each species, and there is no support for a post-Pleistocene population expansion in eastern lineages relative to those from Beringia. Bayesian skyline plots for four of the five species do not support Pleistocene population contraction. Brown Lemmings show evidence of late Quaternary demographic expansion without subsequent population decline. The Wrangell-St. Elias region of eastern Alaska appears to be an important zone of recent secondary contact for nearctic alpine mammals. Despite differences in natural history and ecology, similar phylogeographic histories are supported for all species, suggesting that these, and likely other, alpine- and arctic-adapted taxa are already experiencing population and/or range declines that are likely to synergistically accelerate in the face of rapid climate change. Climate change may therefore be acting as a doubleedged sword that erodes genetic diversity within populations but promotes divergence and the generation of biodiversity. - Center (http://www.uaf.edu/aqc/) David and Rachel Hopkins Fellowship to HCL. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Pleistocene glacial cycles have dramatically shaped the spatial distribution of genetic variation in many species [1]. These massive shifts in climate drove repeated cycles of population contraction and expansion, affecting not only the amount of intraspecific genetic diversity but also its spatial distribution (e.g., [2,3]). While observations of the intraspecific effects of past climate cycling are common, species responses to that cycling are by no means uniform in space, time, or scope. Species responses to climate shifts are affected by many factors, including habitat availability, life history, ecology, and demography. As a result, some extant communities may have shifted together in response to glacial cycling, thus sharing similar patterns of intraspecific diversity across species, or they may represent recent assemblages with no Pleistocene analogs [4], in which case intraspecific diversity will be uncorrelated between species. Understanding how and where diversity has been partitioned is fundamental to modeling responses to past climate change and predicting the effects of future change [5]. This is particularly important for alpine- and arctic-adapted species, which may be at disproportinate risk due to warming temperatures [6]. During previous glacial intervals the Laurentide and Cordilleran ice sheets blanketed much of North America, isolating plant and animal species in multiple refugia (Fig. 1). North of the ice sheets was Beringia, the vast ice-free corridor connecting North America and Asia [7,8]. Beringia has strongly influenced both Asian and North American diversity by permitting biotic interchange [9], limiting dispersal [10], and serving as a center of endemism in its own right [1113]. Although Pleistocene speciation models have been rejected for a number of North American taxa (e.g., [14]), including some high-latitude alpine mammals [15], glacial separation and subsequent reunification of populations has resulted in introgression, competition, and/or replacement between divergent lineages within species [1619]. Furthermore, cycles of repeated isolation, localized extirpation, and ensuing recolonization depressed genetic diversity in many northern species relative to their southern relatives [16,20]. In addition to the Beringian refugium, several cryptic northern refugia appear to have played an important role in the recolonization of previously glaciated regions for some cold-tolerant species [17,25]. These areas include easternmost Beringia (Fig. 1D; [23]), nunataks (emergent rock islands surrounded by glaciers and supporting plant and animal life; [26]) found throughout the region, and areas between adjacent ice sheets in northern British Columbia [27] that may have served as refugia for alpine species. Dominated by herbs and shrubs during previous glaciations [24], these regions appear to have maintained Pleistocene populations of alpine plants [28]. Beringian phylogeographic patterns Phylogeographic studies suggest that the majority of the recently colonizing species in eastern Beringia (present-day Alaska) arrived via North America [18,21]. Patterns of gene flow are related to ecology, with cold-adapted species exhibiting more genetic variation and more evidence of Beringian origins, whereas boreal and temperate forest taxa appear to be recent colonizers [17,21,25]. To date, three major phylogeographic patterns have been pro (...truncated)