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.