Evidence for a cryptic species, forested refugia, and dynamic
contact
Significant geographic structure within Pacific martens is consistent
with the Coastal Refugium Hypothesis (CRH; Fig. 3, 4) and supports the
paleoendemic persistence of insular M. caurina in a North Pacific
coastal refugium, potentially located along the western margins of the
Alexander or Haida Gwaii archipelagos. Insular and continental M.
caurina are genetically distinct despite mitochondrial nesting (Fig.
2d; Supplemental Information 5). We estimated American and Pacific pine
martens diverged just over 1 Mya earlier than recent estimates based on
complete mitochondrial genomes (Schwartz et al. 2020), but
consistently predating the LGM. Rapid evolution of mammalian
mitochondrial genomes and microsatellites and evidence of demographic
bottlenecks within M. caurina (Fig. 3) suggest that previous
divergence estimates may be inflated (Cox 2008; Nielsen & Beaumont
2009; Adachi et al. 1993; Goldstein & Pollock 1997; Zhivotovsky
2001). Within M. caurina , insular and continental clades are
geographically discontinuous (Fig. 1) and estimated to have diverged
almost 100 kya (Fig. 3b); however, PSMC date estimates are
sensitive to scaling (mutation rate and generation time). IntraspecificM. caurina divergence predating the most recent interglacial
suggests that insular Pacific martens may have diverged from continental
populations over multiple glacial cycles, perhaps initially in a coastal
refugium and then subsequently on one or more NPC islands and may
represent a cryptic species previously undetected using single or
multi-gene analyses.
Martens rely on deep persistent snow and complex forest structure
(Proulx 1997; Pauli et al. 2013; Manlick et al. 2017;
Martin et al. 2019) for predator avoidance, thermal management,
and efficient locomotion, suggesting that refugial ecosystems capable of
supporting martens would also support forest community assemblages.
Increased consumption of marine prey items (Giannico & Nagorsen 1989),
consistent with morphological shifts within M. caurina (Colellaet al. 2018b), may have enabled persistence within a relatively
small geographic area. A similar dietary shift towards marine food
sources is also reflected in insular NPC wolves (Darimont et al.2009; Muñoz-Fuentes et al. 2010). The insular-continental split
within M. caurina is consistent with signatures from numerous
other NPC paleoendemic mammals (bears, Heaton et al. 1996;
wolves, Weckworth 2005; deer, Latch et al. 2009; ermine, Colellaet al. 2018c; shrews, Demboski & Cook 2001; deer mice, Sawyeret al. 2018) and also evident in the few associated parasites
examined to date (Soboliphyme baturini , Koehler et al.2007, 2009; Hoberg et al. 2012). Chichagof martens harbor
distinctive nematodes that are phylogenetically close to S.
baturini found in other populations of M. caurina , suggestingM. caurina or a ‘ghost’ marten lineage may persist or persisted
on this island until relatively recently (Koehler et al. 2007,
2009; Hoberg et al. 2012). Similarly, POW is hypothesized to have
been originally occupied by endemic M. caurina (Pauli et
al. 2015) and subsequently colonized by translocations of American pine
martens, which included the introduction of as few as 10 (only 4 female)
documented individuals (Paul 2009). Our genomic analyses, however, did
not find a signature of M. caurina alleles in individuals from
POW or Chichagof islands. Instead, each island was genetically aligned
with M. americana (and their translocation source populations):
Chichagof Island with central Alaska and POW with Revillagigedo Island
(Fig. 2 and 3). These genome analyses, although based on few
individuals, suggest that M. caurina were either not present on
these islands prior to translocations of M. americana or that
they were recently replaced or swamped by introduced M.
americana .
Accidental or intentional introductions (Weber et al. 2017)
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) can result in unanticipated
consequences, including hybridization with native species (Todescoet al. 2016) and exchange of parasites (Prenter et al.2004) with unknown evolutionary outcomes. Genetic management strategies
(Thomas et al. 2013; Whiteley et al. 2015) can be informed
through investigations of existing hybrid zones or historical wildlife
translocations that can provide 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). We
detected two hybrid individuals, each collected from a distinct natural
mixing zone: Kuiu Island Alaska and western Montana in the northern
Rocky Mountains (Table 2; Fig. 2-4; Supplemental Information 9-16). Both
hybrids were female, had M. americana mitochondrial haplotypes
(Fig. 2d), and mixed nuclear ancestry, with the Montana hybrid
containing continental M. caurina alleles and the Kuiu hybrid
containing insular M. caurina alleles (Table 2; Supplemental
Information 10-13, 16-17). Both admixed individuals were identified as
early generational-stage hybrids (e.g., F1’s or a single generation
backcrossed with M. americana , Supplemental Information 11-12)
with introgression occurring recently (Supplemental Information 21).
Although sample sizes are small, the absence of late-generational
hybrids is surprising, especially for the Montana zone which has
persisted for many generations (Wright 1953). Detection of only
early-generational hybrids is consistent with the presence of hybrid
incompatibilities, where F1 hybrids experience a temporary elevation in
fitness (heterosis) compared to later generational-stage hybrids (e.g.,
F2 and beyond) that may suffer outbreeding depression as a result of
disrupted co-adapted gene complexes (Todesco et al. 2016). The
disruption of co-adapted gene complexes or genes involved in local
adaptation via introgression, and particularly loci involved in disease
and pathogen resistance (Alibert et al. 1994), may pose a
particular challenge to naïve insular taxa. This hypothesis warrants
further genomic investigation with expanded and fine-scale sampling from
within hybrid zones and translocated islands.
Within M. americana , Chichagof Island exhibits the highest
effective population size (Ne), followed by central
Alaska (Fig. 3b). Although high Ne is surprising for an
insular population, Chichagof Island received iterative translocations
of M. americana in the mid-1900s from multiple source
populations, including four other islands in southeast Alaska (Baranof,
Wrangell, Mitkof [Petersburg], and Revillagigedo [Ketchikan]
islands) and one distant continental locality (Polly Creek, in central
AK). Those introductions likely inflate population size estimates as a
consequence of outbreeding (Paul 2009) and make the historical
distribution of Ne for this individual resemble that of
mainland populations (e.g., MAK). In contrast, Prince of Wales Island
(POW) received introductions from only two proximate sources:
Revillagigedo and Mitkof islands (Burris & McKnight 1973; Paul 2009).
Revillagigedo Island shows a similar demographic history to POW,
suggesting those translocations resulted in successful establishment
(Elkins & Nelson 1954). Absence of M. caurina alleles on POW or
Chichagof suggests that interspecific competition, outbreeding, or the
introduction of foreign pathogens among other variables may have
impacted endemic M. caurina (Plein et al. 2016; Colellaet al. 2018b; Northover et al. 2018). Ultimately, until
additional hybrids are sequenced, our results discourage further
wildlife translocations into the NPC islands due to potential swamping
and emphasize the importance of careful source population selection for
genetic rescue, as the NPC harbors significant cryptic diversity that
represents complex evolutionary histories.