ECR feature: Jocelyn P. Colella on the persistence of forest‐associated mammals in refugia

Jocelyn P. Colella is a Postdoc at the University of New Hampshire. She is an evolutionary biologist applying collection-based data to understand how organisms change through time. Here, Jocelyn shares her recent work that uses whole‐genome resequencing to reveal the persistence of martens in Late Pleistocene refugia along North America’s North Pacific Coast.

Jocelyn doing fieldwork in Panama (Photo by friend and colleague: Schuyler Liphardt)

Personal links. Personal website | Twitter

Institute. Molecular, Cellular and Biomedical Sciences Department, University of New Hampshire

Academic life stage. Postdoc

Major research themes. Hybridization and adaptation in mammals

Pacific marten (Martes caurina) (Photo by L. L. Master courtesy of the Mammal Image Library).

Current study system. Martens (Martes spp.) are medium-sized carnivores belonging to the weasel family (Mustelidae). In North America, marten fur is important to northern economies, but population sizes have been decreasing. In response, martens have been translocated or moved around to augment or restore native populations, but often without an understanding of native diversity. In addition to their tubular body shape and reputation as voracious predators, I think one of the coolest adaptations of the Mustelidae family is the ability to pause embryonic development (a process called embryonic diapause) until environmental conditions are conducive to raising young.

Recent paper in JBI. JP Colella, T Lan, SL Talbot, C Lindqvist, JA Cook. (2021). Whole-genome resequencing reveals persistence of forest-associated mammals in late Pleistocene refugia along North America’s North Pacific Coast. Journal of Biogeography, 48(5), 1153-1169.

Jocelyn and Dianna Kreja (new Curator of Mammals at the University of Wisconsin Zoological Museum) collecting mammals in the Gila Wilderness of New Mexico.

Motivation behind this paper. A number of “glacial refugia” or ice-free areas are proposed along the western edges of North America’s North Pacific Coast. Ocean and climate modelling and sediment cores suggest that refugial areas were mostly tundra during the peak of the last glaciation, and therefore devoid of most plants and animals, but investigations into the genomes of coastal species have found increasing support for complex and diverse refugial communities. Martens (Martes spp.) are ‘forest associated’ mammalian carnivores that require complex, structured forests to complete their life-cycles. Therefore evidence of refugial persistence in martens can inform the composition and distribution of historical paleoenvironmnets. Pacific martens are native to three islands along the North Pacific coast and come into contact with American pine martens along the coastline, which provides an opportunity for secondary contact and the exchange of genetic material. Economically motivated wildlife translocations in the mid-1900s also provide opportunities for hybridization, which is most easily examined from a genomic perspective. Thus, we aimed to test (i) whether martens were historically present in North Pacific coastal refugia and (ii) the impact of hybridization on the evolution and continued conservation and management of these species.

Key methodologies. We used whole-genome resequencing of two marten species: American pine martens (Martes americana) which are distributed throughout continental North America and Pacific martens (Martes caurina) which have a disjunct distribution on a few North Pacific Coast islands and also on sky-islands in the American West. We mapped genomic reads to the domestic ferret genome to assess the evolutionary, demographic, and hybrid histories of these species. This is the first time genomic data has been generated for North American martens, although chromosome level assemblies for near relatives are starting to emerge through DNAzoo (Wahoo!). Whole-genome resequencing allows us to characterize demographic histories using methodologies such as Pairwise Sequential Markovian Coalescence (PSMC) which illustrates how population sizes have changed over deep time (millions of years). The many variable sites available through the genomes allowed fine-scale analysis of introgression or gene flow which we expected to occur in known contact zones (one along the coast and another in the northern Rocky Mountains). The directionality, frequency, and timing of gene flow help outline the consequences of genetic mixing: do we expect the two species to fuse into one? Or will interbreeding lead to the swamping or loss of one species and not the other?

Ventral aspect of an American pine marten skull collected on Baranof Island, Alaska (Photo by Jocelyn P. Collela).

Unexpected challenges. Since marten hybridization and translocation histories motivated this work, we expected to find more evidence of gene flow. Yet, evidence of hybridization was only found for two individuals, each collected within a known hybrid zone. Interestingly, both hybrids appear to be F1’s or first-generation hybrids between Pacific and American pine martens. This is unusual because if hybridization is common, we would expect to see many individuals with varying ancestry proportions and we don’t! So perhaps hybridization is not as common as we suspected? The next question is: Why?

Major results. We discovered two lineages of Pacific marten: one insular and one continental. Our results support a deep history of insular Pacific martens (>100,000 years ago) along the North Pacific Coast consistent with refugial isolation along the coast. Evidence of forest-associated mammals, like martens, along the North Pacific Coast suggests that paleoenvironments of coastal refugia were more complex than previously thought, containing martens, but also possibly sparse forests and a sufficient small mammal prey base to sustain mesocarnivores.  We identified two early-generational hybrids (F1’s), one in each known contact zone. Both hybrids had American pine marten mitochondrial DNA and mixed nuclear DNA, consistent with a bias in the directionality of hybridization, which may negatively impact the persistence of Pacific martens.

Jocelyn tying a museum tag onto a wolverine (Gulo gulo) skull in Northwest Territories Canada. Many of the samples used in this work and others are donated to museums by wildlife agencies, hunters, and trappers (Photo by friend and colleague Dianna Krejsa).

Next steps for this research. Based on these genomes, it looks as though the insular Pacific marten may be a distinct species. The next step would be to increase genetic sample sizes and rigorously evaluate morphological differences to test the species status of the Pacific marten lineages. We also need to take a closer look at each hybrid zone and determine admixture proportions among a larger number of individuals to determine the frequency and geographic distributions of different levels of hybrids (e.g., F1, F2, backcross).

If you could study any organism on Earth, what would it be? I’m all about mammals, big or small. As a now-retired NCAA swimmer and current avid “Master’s” swimmer, I suppose I’m partial to marine and semi-aquatic mammals: otters (also weasels!), muskrats, beavers, pinnipeds (seals, sea lions), and cetaceans (whales, dolphins). Due to the lack of physical barriers to movement in oceans, I find speciation and hybridization dynamics in these systems to be both fascinating and unusual, and wonder if the evolution of marine mammals may parallel that of volant (or flying) mammals, like bats.

Selfie during 2019 Summer field work in the Mojave desert, holding a kangaroo rat (Dipodomys merriami).

Anything else to add? Complex biotic communities along the North Pacific Coast may have also provided resources to sea-faring humans en route to the Americas. Industrial scale logging of old-growth forests and road development in the Tongass National Forest within the North Pacific Coast also poses a risk to insular Pacific martens by shrinking available habitat. Southwestern sky island habitat is further shrinking in response to climate change, placing Pacific martens at risk of extinction or extirpation.

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