Coastal Paleoenvironments
Disparate distributions of insular lineages across these heterogeneous archipelagos suggests that the geographic pattern and duration of refugial isolation may vary across climate cycles, depending on the ecological plasticity and dispersal abilities of incumbent species (Colella et al. 2018c; Slager et al. 2020). Insular ‘ABC’ brown bears (Ursus arctos, Heaton et al. 1996), for example, are currently geographically restricted to the three northern most islands of the Alexander Archipelago (Admiralty, Baranof, Chichagof), while the insular black bear lineage (Byun et al.1997) has a more southerly distribution encompassing southern Alexander Archipelago islands, the Haida Gwaii Archipelago, Vancouver Island, and coastal British Columbia. Under the assumption of niche conservatism, this phylogeographic pattern suggests a cooler, northern refugium within the Alexander Archipelago and a slightly warmer, perhaps more heavily vegetated refugial ecosystem to the south, either in the southern Alexander Archipelago or Haida Gwaii. Early paleoclimatic models for NPC refugia hypothesized these areas to be primarily tundra and unable to support forest-associated taxa such as black bears and martens (Barrieet al. 1993; Mann & Hamilton 1995; Hansen & Engstrom 1996; Ager 2007). However, recent palynological investigations and radiocarbon dating of postglacial peat and sediment cores indicate instead that coastal forests similar to today’s forests existed in the Alexander Archipelago during the last interglacial (Ager 2019). Rapid colonization of the western-most islands by spruce (Picea ) immediately following glacial recession (~17 kya) hints at the potential refugial persistence of coniferous forests (Lesnek et al. 2018; Ager 2019) and parallels our hypothesis that refugial persistence of insular M. caurina is more likely than post-glacial recolonization, given the poor oceanic dispersal capabilities of this species and significant differentiation from mainland counterparts. Refugial divergence of insular M. caurinaalong the NPC also explains the disjunct contemporary distribution of this species (Fig. 1). Along the NPC, M. caurina inhabits at least three islands; however, Admiralty Island in Southeast Alaska is more than 300 km north of the two insular Canadian populations. Although geographic disjunction across three islands is substantial, the genetic similarly of these island populations points to historical divergence in a single coastal refugium and a potentially more widespread historical distribution of insular M. caurina throughout NPC islands. Higher density sampling across the NPC will be necessary to refine the geographic limits of insular and continental M. caurina clades and the genomic data generated here provide a foundation for generating species-diagnostic SNP panels for such investigations.
Comparative demography also identified at least three major evolutionary trajectories: M. americana and insular and continental M. caurina (Fig. 3b), again consistent with the CRH. Effective population sizes of American pine marten are overall higher than those of M. caurina , consistent with the contiguous contemporary range of this species and historical divergence in and subsequent expansion from a single, large eastern refugium (Stone et al. 2002). Although our results hint at insular-continental structure within M. americana(Fig. 3), this signal is muddled by historical wildlife translocations and remains unresolved from a nuclear perspective (Fig. 2). Relative toM. americana , both M. caurina lineages have consistently smaller effective population sizes. Insular M. caurina in particular show a significantly depressed effective population size through time and the highest overall inbreeding coefficients. Although likely a consequence of island life, small effective population sizes and high levels of inbreeding place insular martens at an elevated risk of extinction (Frankham 1998; Rybicki & Hanski 2013), which is especially relevant in the face of proposed environmental modifications to the Tongass National Forest (Stewart 2016).
Our genomic results initially appear to contradict the fossil record, which shows a scarcity of fossils on POW Island during the LGM (~20-15 kya, Lesnek et al. 2018) and documents martens appearing on POW during the late Pleistocene (>14 kya) and early Holocene (9-14 kya, Heaton & Grady 2003; Pauli et al. 2015). However, the absence of martens and other mammals in the Southeast Alaskan fossil record during the LGM may reflect sampling bias, as most dated fossil materials from the region were collected from the Shuká Káa cave at the northern end of POW (Heaton 2002). InsularM. caurina have not been documented on POW and this site was likely ice-covered at the peak of the LGM (Lesnek et al. 2018). Even so, a number of meso-carnivore teeth from Shuká Káa cave morphologically identified as mink (Mustela vison ) may instead mark the early presence of insular M. caurina (Heaton & Grady 2003), as these species have similar tooth morphology and these tentative identities should be confirmed. Similar to misidentifications of Pleistocene coastal black bear (Ursus americanus ), fossils from POW as brown bears (Ursus arctos ) due to size differences over evolutionary timescales (Lindqvist pers. obs.), insularM. caurina are physically larger than both M. americanaand continental M. caurina (Colella et al. 2018b) which may confound historical taxonomic assignment by dentition. Persistence of diverse communities of large terrestrial mammals, including caribou, bears, and foxes, evident in the fossil record both pre- and post-LGM (Lesnek et al. 2018), points to a higher potential for local refugial persistence through the LGM over the recolonization of these outer islands from mainland sources since the Holocene (Ager 2019).
The viability of a coastal migration route for human colonization of the Americas hinges on our understanding of glacial extent and biotic community composition along the NPC during the late Pleistocene. Similar to martens, access to both marine and terrestrial prey items and timber resources along a NPC migration route, would have enhanced human survivorship during an early pulse of human migration into the Americas via the Pacific coast (Fladmark 1979; Dixon 1993). Geological investigations of hypothesized coastal refugia in southeast Alaska have produced mixed results. Bathymetry (Carrara et al. 2003, 2007) and palynology (Barrie et al. 1993; Mann & Hamilton 1995; Ager 2019) support the persistence of coastal refugia of varying complexities. In contrast, preliminary cosmogenic exposure dating has raised doubt on hypothesized refugial locations (Lesnek et al.2018). Consistent signatures of refugial persistence across taxa (Foster 1965; Heaton et al. 1996; Hewitt 2000, 2003; Weckworth et al. 2005; Colella et al. 2018c; Sawyer et al. 2018; Slager et al. 2020) and the rapid colonization of glaciated regions followed glacial recession supports the persistence of complex refugial communities along the coast. Our results suggest the persistence of a forest-associated meso-carnivore along the NPC through the LGM, despite the absence of this species in the fossil record.
Differentiation between insular and continental M. caurina was suggested previously based on a limited set of loci (Demboski et al. 1999, 2001; Stone et al. 2002; Small et al. 2003; Dawson et al. 2017), but the extent and timing of divergence and potential effects of repeated contact were unknown. The genomic signature of refugial divergence and subsequent contact found here may be more widespread than previously suspected, with additional forest-associated taxa, not well represented in the fossil record or yet examined with genome scale data, also persistent in NPC refugia. Our results underscore the importance of reevaluating work previously based on one or a few genes, as genomic resolution invariably provides more detailed and often unexpected insights into the evolutionary complexities of coastal refugia (Miller et al. 2012; Colellaet al. 2018c) and holds great promise to unravel complexity across space and time.