INTRODUCTION
Centers of endemism and geographically clustered hybrid zones are hypothesized to be the legacy of species persistence through the Pleistocene in multiple ice-free glacial refugia followed by population expansion and contact (Hultén 1937; Heusser 1989; Heaton & Grady 2003; Swenson & Howard 2005). Isostatic adjustment and lower sea-levels (Mann 1986) are credited with exposing areas of the continental shelf along North America’s North Pacific Coast (NPC) and providing terrestrial sanctuary for insular and coastal species displaced by the expanding Cordilleran and Laurentide ice sheets (Heaton et al. 1996; Hewitt 2000; Lacourse et al. 2003; Mathewes & Clague 2017). Multiple refugia are hypothesized within southeast Alaska’s contemporary Alexander Archipelago (e.g., Baranof, Chichagof, Dall, Heceta, and Prince of Wales islands; Foster 1965; Fedorov & Stenseth 2002; Carrara et al. 2003, 2007; Ager 2019) and British Columbia’s Haida Gwaii Archipelago and surrounding areas (Heusser 1989; Mathewes & Clague 2017). Ice-free coastal refugia may have also played an integral role in human colonization of the Americas by opening a maritime migration corridor. New evidence shows the Pacific Northwest was inhabited by humans as early as > 15-16 thousand years ago (kya; Devièseet al. 2018; Davis et al. 2019) and the Alexander Archipelago at least > 10 kya, but likely more than 13 kya (Dixon et al. 2014; Carlson & Baichtal 2015; Lesnek et al. 2018; Mackie et al. 2018; McLaren et al. 2018), potentially predating the opening of an ice-free migration corridor through central Alberta, Canada (<=14.8 kya; Margold et al. 2019). An incomplete fossil record, however, creates uncertainty over which species persisted in hypothesized refugia, obscuring interpretation of their duration and paleoenvironments. Unlike humans with access to rudimentary sea-faring technologies (Erlandson et al. 2007), other coastal refugial mammals would have been essentially isolated from mainland populations, leading to a cessation in gene flow and divergence over time (Hewitt 2000). As such, the genomes of refugial descendants can provide clues to whether populations or species diverged in refugial isolation. Predicted variation includes high genetic differentiation from other refugial populations and the abundance of endemic or ancestral alleles, low genetic diversity as a consequences of small population sizes and genetic drift, and less spatial structure relative to recently colonized populations (Hewitt 2000).
In contrast to glacial isolation, post-glacial population expansion from multiple refugia can lead to secondary contact and the formation of hybrid zones between previously isolated taxa (Hewitt 2000; Swenson & Howard 2005). The rapid climatic oscillations of the Pleistocene (Williams 1998) led to recurrent opportunities for contact and gene flow between incompletely diverged taxa (Hewitt 2000, 2003). The consequences of genetic exchange are complex and range from homogenization to hybrid speciation (Arnold 1997; Harrison & Harrison 1993; Genovart 2009; Abbott et al. 2016), depending on the level of differentiation, but they can now be examined in detail using whole-genome sequences (Twyford & Ennos 2012).
North American martens are relatively small meso-carnivores, hypothesized to have diverged in at least two independent glacial refugia south of the Laurentide ice sheet (Stone et al. 2002): one refugium east of the Rocky Mountains or Mississippi River drainage giving rise to American pine martens (Martes americana , Turton 1806) and another to the west, presumably the cradle for Pacific martens (Martes caurina , Merriam 1890). However, the disjunct contemporary range of Pacific martens and occurrence of two natural hybrid zones between these species\(\ \) one occurring on near-coastal islands (Kuiu and Kupreanof, AK) along the NPC and another in the northern Rocky Mountains (Fig. 1)\(\ \) suggest Pacific martens may have a deeper evolutionary history along the NPC than previously thought (Pauli et al. 2015). The widespread coast-to-coast boreal distribution of M. americana directly contrasts with the fragmented distribution of M. caurina, found along the Pacific coast (CA, OR, WA), mountaintops of the American Southwest (NM, CO, UT) and northward into Montana and Idaho, and four islands within the putative refugial archipelagos of the NPC: Graham, Moresby, Kuiu, and Admiralty islands.
In addition to two natural hybrid zones, a series of intentional wildlife translocations in the mid-1900s introduced M. americanato multiple NPC islands without prior knowledge of the native marten species in the region (Powell et al. 2012). While these introductions may complicate the interpretation of genomic signals from this region, they also provide a framework for interpreting the consequence of natural versus anthropogenically-mediated gene flow on the evolution and persistence of species. Accidental introductions (Fenichel et al. 2008; Weber et al. 2017) or intentional, motivated by economics (McNeely 2001; Fenichel et al. 2008; Powell et al. 2012), public safety (Massei et al. 2010) or conservation (Powell et al. 2012), are increasingly common and can result in unanticipated consequences, including hybridization with native species (Todesco et al. 2016) and exchange of parasites (Prenter et al. 2004) with unknown evolutionary outcomes. Genetic management techniques, including genetic rescue (Whiteley et al.2015) or gene tweaking (Thomas et al. 2013), are increasingly proposed as viable mechanisms to boost diversity in small inbred populations. Application of these techniques can be informed through investigations of existing hybrid zones and historical wildlife translocations which can cumulatively inform a predictive framework for anticipating the evolutionary consequences of genetic exchange. In martens, hybridization may disproportionately impact Pacific martens through genetic dilution from outbreeding (Colella et al. 2018a). Low genetic variation in certain insular populations of M. caurina (Stone et al. 2002; Small et al. 2003) has led to further concerns over their persistence, which may be exacerbated by ongoing harvest of forests and extraction of minerals on those islands (Durbin 1999; USDA 2018).
We use whole-genome resequencing data to refine our understanding of the biogeographic history of NPC martens and place these results within the context of the Coastal Refugium Hypothesis (CRH; Heusser 1989; Scudder & Gessler 1989; Heaton et al. 1996; Demboski et al. 1999; Sawyer et al. 2019). With increased molecular resolution, we explore the evolutionary consequences of introgression in New WorldMartes to further inform natural resource management initiatives. We examine the distribution of geographic variation and estimate the timing and directionality of introgression to assess the role of natural hybridization, historic wildlife translocations, natural colonization events, and glacial cycling in shaping the evolution of New World martens.