Whole‐genome resequencing reveals persistence of forest‐associated mammals in Late Pleistocene refugia along North America’s North Pacific Coast

Abstract

Aim: Numerous glacial refugia have been hypothesized along North America's North Pacific Coast that may have increased divergence of refugial taxa, leading to elevated endemism and subsequently clustered hybrid zones following deglaciation. The locations and community composition of these ice-free areas remains controversial, but whole-genome sequences now enable detailed analysis of the demographic and evolutionary histories of refugial taxa. Here, we use genomic data to test spatial and temporal processes of diversification among martens with respect to the Coastal Refugium Hypothesis, to understand the role of climate cycling in shaping diversity across complex landscapes.Location: North America and North Pacific Coast archipelagos. Taxon: North American martens (Martes).Methods: Short-read whole-genome resequencing data were generated for 11 martens: four M. americana, four M. caurina, two hybrids, and one outgroup (Martes zibellina). Sampling was representative of known genetic clades within New World martens, including sampling within insular and continental hybrid zones and along the North Pacific Coast (five island populations). ADMIXTURE, F-statistics, and Dstatistics (ABBA-BABA) were used to identify introgression and infer directionality.Heterozygosity densities, estimated via PSMC, were used to characterize historical demography at and below the species level to infer refugial and colonization processes. Results: Forest-associated Pacific martens (M. caurina) are divided into distinct insular and continental clades consistent with the Coastal Refugium Hypothesis. There was no evidence of introgression on islands that received historical translocations of American pine martens (M. americana), but introgression was detected in two active zones of secondary contact: one insular and one continental. Only early-generational hybrids were identified across multiple hybrid zones, a pattern consistent with potential genetic swamping of M. caurina by M. americana. Main conclusions: Despite an incomplete fossil record, genomic evidence supports the persistence of forest-associated martens, likely the insular Pacific marten lineage, along the western edges of the Alexander Archipelago during the Last Glacial Maximum. This discovery informs our understanding of refugial paleoenvironments,

Speciation without gene‐flow in hybridizing deer

“…The dynamic history of the North American continent, notably the glacial cycles of the Quaternary, shaped the evolution and distribution of many taxa (Avise et al, 1998; Hewitt, 2000; Shafer et al, 2010). The use of different refugia for prolonged periods of time during the glaciation events has increased the differentiation between populations in several species, including deer (Colella et al, 2021; Dussex et al, 2020; Ito et al, 2021; Kinoshita et al, 2020; Latch et al, 2014). Previous studies show that MD persisted in several refugia during the glacial cycles of the Pleistocene, increasing the intraspecific divergence (Latch et al, 2009, 2014; Wright et al, 2022).…”

Speciation without gene-flow in hybridising deer

“…The dynamic history of the North American continent, notably the glacial cycles of the Quaternary, shaped the evolution and distribution of many species (Avise et al 1998; Hewitt 2000; Shafer et al 2010). The use of different refugia for prolonged periods of time during the glaciation events has increased the differentiation between populations in several species, including deer (Latch et al 2014; Dussex et al 2020; Kinoshita et al 2020; Colella et al 2021; Ito et al 2021). Previous studies show that MD persisted in several refugia during the glacial cycles of the Pleistocene, increasing the intraspecific divergence (Latch et al 2009; Latch et al 2014; Wright et al 2022).…”

“…Hewitt, 2000;Shafer et al, 2010). The use of different refugia for prolonged periods of time during the glaciation events has increased the differentiation between populations in several species, including deer (Colella et al, 2021;Dussex et al, 2020;Ito et al, 2021;Kinoshita et al, 2020;Latch et al, 2014). Previous studies show that MD persisted in several refugia during the glacial cycles of the Pleistocene, increasing the intraspecific divergence (Latch et al, 2009(Latch et al, , 2014Wright et al, 2022).…”

Ancient bears provide insights into Pleistocene ice age refugia in Southeast Alaska

“…However, given the rapid sea-level rise following the glacial retreat in SE Alaska, it is possible that refugia were available in areas of the now-submerged continental shelf (Baichtal et al, 2021;Walcott et al, 2022) and that smaller species with small home ranges, such as Pacific marten (Colella et al, 2021)…”

“…Although the validity of some of these endemics has been questioned (MacDonald & Cook, 2007), several island or coastal endemics belong to distinct genetic lineages when compared to continental populations found farther east (Cook et al, 2006; Sawyer et al, 2019). Examples include American black bear ( Ursus americanus ), brown bear ( U. arctos ), Pacific marten ( Martes caurina ), Haida ermine ( Mustela haidarum ) and several small mammals (Byun et al, 1997; Colella et al, 2018, 2021; Cook et al, 2006; Dawson et al, 2014; Hope et al, 2016; Jackson & Cook, 2019; Puckett et al, 2015; Sawyer et al, 2019; Talbot & Shields, 1996; Wooding & Ward, 1997). Extensive paleontological work in the Alexander Archipelago recovered thousands of mammalian remains from multiple caves, including human remains and artefacts (Aqil et al, 2023; Dixon, 2015; Lindo et al, 2017), and some of the oldest New World dog remains (da Silva Coelho et al, 2021).…”