High-latitude diversification within Eurasian least shrews and Alaska tiny shrews (Soricidae)

Abstract A novel shrew was discovered recently in Alaska and described based on morphological characters as Sorex yukonicus. This species is closely allied to Sorex minutissimus, a widespread shrew ranging through Eurasia. Together their distribution spans Beringia, a large Pleistocene nonglaciated area that connected Asia and North America. Beringia was repeatedly divided due to raised sea levels during Pleistocene interglacials and subsequently reconnected during glacials. We tested predictions related to the influence of large-scale geologic events on genetic variability through a phylogeographic analysis of both species of shrew using evidence from 3 independent genetic loci. We found low genetic divergence between S. minutissimus and S. yukonicus across continents. However, major phylogeographic breaks were found for Eurasian and Maritime Northeast Asia populations. Neither species is reciprocally monophyletic for any of the loci examined. Coalescence times for all pairwise population comparisons within both species fall within the Wisconsinan–Weichselian glacial (<130 thousand years ago), and significant population expansion estimates date to the Holocene suggesting that divergence between these taxa is minimal and may not warrant recognition of 2 distinct species. Phylogeographic relationships and sequence divergence estimates place populations of North American S. yukonicus and Siberian S. minutissimus as most closely related, and together they are sister to European S. minutissimus. We conclude that populations east and west of the Bering Strait represent a single Holarctic species, S. minutissimus. Temporal changes in range based on ecological niche predictions and a comparative assessment of other codistributed taxa provide a preliminary view of potential Last Glacial Maximum refugia in northern Asia. Bayesian skyline plot, Beringia, ecological niche model, multiple loci, phylogeography, Pleistocene refugia, Sorex minutissimus, Sorex yukonicus Climatic variability during the Pleistocene had a major impact on the evolution and distribution of high-latitude species (Hewitt 1996, 2004), with >20 significant glacial cycles recorded during this epoch (Williams et al. 1998). Northern species experienced major range shifts involving contractions into discrete refugia and subsequent expansions as they recolonized deglaciated areas (Schmitt 2007). The record of these demographic changes through repeated climatic cycles often is obscured by the actions of the most-recent glacial cycle, effectively wiping the historical slate clean (Avise 2000); however, sometimes the signature of past glaciations persists through multiple glacial events (Lu et al. 2001; Runck et al. 2009). Fossil remains are independent evidence of previous occupation but provide only a minimum time estimate of geographic occupation. For many small mammals, fossils often are not available or are difficult to identify (Near and Sanderson 2004; Smith and Peterson 2002). Geographic distributions coupled with knowledge of geologic and climate change through time can be compared with morphologic or genetic information from extant populations to infer the history of diversification and spatiotemporal change within and among species (Lister 2004). In Europe, species occupied putative southern refugia during glacial maxima, and many recolonized northward following retreat of the Fennoscandian ice sheet in response to a wanning climate (Hewitt 2001; Schmitt 2007). In addition, genetic signatures of other newly recognized refugia situated further east in Europe (e.g., Carpathians—Provan and Bennett 2008) also have been identified and implicated as sources for westward recolonization (Fedorov et al. 2008; Hewitt 2004). Likewise, most of northern North America was covered by the Cordilleran and Laurentide ice sheets. Following deglaciation, species that were pushed south subsequently expanded north to occupy newly exposed land (Runck and Cook 2005). In contrast, much of eastern Europe, Siberia, and northwestern North America remained virtually ice-free from the Taimyr Peninsula eastward across Beringia to the Mackenzie Mountains in the Yukon (Hopkins 1967; Svendsen et al. 2004), and yet phylogeographic patterns for high-latitude species occupying North America and East Asia remain poorly understood. Heterogeneous topography including mountain ranges, large rivers, and lakes, coupled with variable climatic cycles, fragmented this immense region into discrete xeric or mesic refugia (Ehrich et al. 2008; Fedorov et al. 2008; Mangerud et al. 2004). Beringia is perhaps the most recognized ice-free refuge at high latitudes (Abbott and Brochmann 2003; Hultén 1937). During glacial maxima lowered sea levels exposed a land bridge between Asia and North America effectively extending Asia eastward to the western limits of the North American ice sheets and allowing for continental exchange of terrestrial biota (DeChaine 2008; Elias and Crocker 2008; Sher 1999). During glacial episodes species from Asia could pass into eastern Beringia (central Alaska and northwestern Yukon), whereas North American species were restricted to lower latitudes south of continental ice sheets. Consequently, most known intercontinental movements of species across Beringia are eastward, although notable exceptions include some shrews (Waltari et al. 2007b). Species and complexes that span the nexus between Asia and North America provide a window into the historical biogeography of faunal exchanges. The Alaska tiny shrew, Sorex yukonicus (Dokuchaev, 1997), was described from previously misidentified museum specimens. Originally thought to be the Eurasian least shrew, S. minutissimus (Dokuchaev 1994), these specimens were later elevated to a new species based on morphological differences (Dokuchaev 1997). Dokuchaev (1997) suggested that S. minutissimus invaded Alaska prior to the Illinoian glacial and then diverged within Beringia as S. yukonicus during the Illinoian (0.21–0.13 million years ago [mya]). Although morphological differences were detected with principal component analysis, the study by Dokuchaev (1997) was based on a limited number of samples (6 individuals). Since that study an additional 27 specimens have been archived, all within the confines of Alaska. The geographic range of S. minutissimus is broad, extending from Scandinavia eastward across Asia to the Bering Strait and as far south as Mongolia and southeast to Primorsky Krai and Japan (Ohdachi et al. 2001; Sheftel 2005). The least shrew inhabits forest–tundra, taiga, forest–steppe, and dry steppe habitats (Yudin 1971). Other taxa (e.g., arthropods, birds, fish, parasites, and plants) also exhibit broad Holarctic distributions (Fedorov et al. 2008; Haukisalmi et al. 2004, 2009; Hewitt 2004; Waltari et al. 2007b). Distinctive phylogeographic breaks are common among high-latitude mammals including an east–west split in the vicinity of the Ural Mountains of western Russia (...truncated)