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Map of North American marten distributions (M. americana range in green, M. caurina in blue) with natural hybrid zones denoted by yellow hatching and islands that received translocations of M. americana outlined in heavy black (CHI, BAR, POW). Three letter localities codes correspond to population abbreviations in Table 1. Each dot represents a sampled specimen, colored by mitochondrial species assignment: M. americana in green, M. caurina in blue, with putative hybrids colored based on mtDNA assignment and identified by a yellow ‘X’
Source publication
The evolutionary consequences of natural introgression provide a rare opportunity to retrospectively evaluate how the introduction of exotics or genetic rescue efforts may impact endemic faunas. Phylogeographic structure among mainland, endemic insular, and introduced North American marten (Martes americana and M. caurina) populations have been sha...
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Citations
... Hybridization is a consequential process that impacts evolution in a diversity of ways. For example, hybridization can introduce reticulated patterns of evolution (Larsen et al. 2010), and lead to a variety of detrimental effects such as outbreeding depression (Beauclerc et al. 2013), genetic swamping (Colella et al. 2018), and the accumulation of deleterious variation (Pfennig 2021). However, introgressive hybridization can also introduce novel genetic material for parental species, increasing genetic variation and potentially contributing to adaptive evolution (Hamilton and Miller 2016;Jones et al. 2018). ...
Hybridization is a common process that has broadly impacted the evolution of multicellular eukaryotes; however, how ecological factors influence this process remains poorly understood. Here, we report the findings of a 3-year recapture study of the Bryant’s woodrat (Neotoma bryanti) and desert woodrat (N. lepida), two species that hybridize within a creosote bush (Larrea tridentata) shrubland in Whitewater, CA, USA. We used a genotype-by-sequencing approach to characterize the ancestry distribution of individuals across this hybrid zone coupled with Cormack-Jolly-Seber modeling to describe demography. We identified a high frequency of hybridization at this site with ~40% of individuals possessing admixed ancestry, which is the result of multigenerational backcrossing and advanced hybrid-hybrid crossing. F1, F2 and advanced generation hybrids had apparent survival rates similar to parental N. bryanti, while parental and backcross N. lepida had lower apparent survival rates and were far less abundant. Compared to bimodal hybrid zones where hybrids are often rare and selected against, we find that hybrids at Whitewater are common and have comparable survival to the dominant parental species, N. bryanti. The frequency of hybridization at Whitewater is therefore likely limited by the abundance of the less common parental species, N. lepida, rather than selection against hybrids.
... More recently, these Martes taxa were revised into specific status via molecular approaches (Stone & Cook 2002). In the few places where American and Pacific martens are in contact, they have been shown to hybridise (Colella et al. 2019), which has even led to where martens occur without fishers (hatched lines represent overlap between Martes americana and Martes caurina); yellow fill for where fishers occur without martens; green is regions of sympatry, where both species occur. Also provided are numbered locations of reviewed papers that explored marten and fisher niche overlap in: 1) California, USA ; 2) Alberta, Canada (Fisher et al. 2013); 3) Manitoba, Canada (Raine 1972); 4) Minnesota, USA 5) Wisconsin, USA (Manlick et al. 2017b; 6) Michigan, USA (Croose et al. 2019); 7) Quebec, Canada (Suffice et al. 2020); 8) New York, USA (Jensen & Humphries 2019); and 9) Maine, USA (Krohn et al. 1995). ...
Competition is a major determinant of where species occur and how species interact. Among carnivorans, interspecific competition is particularly apparent, as many of these species have evolved to be efficient killers. Theoretically, phylogenetically related carnivorans that occupy seasonal habitats, share common resources, and differ in body size by a factor of 2.5–10× should exhibit the most interference competition. Fishers Pekania pennanti and martens Martes americana and Martes caurina are members of the subfamily Guloninae (Mustelidae, Carnivora) that occupy forests throughout northern North America. These taxa occur sympatrically throughout much of their range, utilise similar habitats, and consume similar prey; fishers and martens also differ in body size by a factor 2–5×. Consequently, these two taxa appear to be locked in particularly strong interspecific competition and should attempt to limit competitive overlap. We review the current knowledge of this dyadic interaction in the framework of ecological niches and niche partitioning. In particular, we explore the three critical niche axes of diet, space, and time. We found that, in contrast to the traditional view of them being highly specialised, both martens and fishers are dietary generalists; however, they also appear to be specialists in complexity, at least in space and habitats. Collectively, martens and fishers exhibit high degrees of diet and habitat niche overlap across their ranges, and this overlap is likely to have the greatest fitness consequences for the smaller and subordinate martens. Nevertheless, fine‐scale habitat and prey partitioning, and especially partitioning along snow clines, seem to be the mechanisms by which these two taxa can coexist. We predict that rapid ecological change – especially from increasingly homogenised forests and prey communities, as well as from declining snow cover and snowpack due to climate warming – is likely to destabilise marten–fisher coexistence. As the climate continues to change, fishers and martens are likely to experience distributional and numerical shifts and increased isolation at their southern range boundaries, and vulnerable populations – especially of martens – will be driven to local extirpation. Martens Martes americana and Martes caurina and fishers Pekania pennanti are closely related and similar‐sized species that exhibit broad range overlap across North America and use similar habitats and resources. Based on first principles, then, these species should exhibit pronounced interspecific competition and exclusion. Herein, we synthesised the current state of knowledge for these competing species utilising a large volume of peer‐reviewed literature. We found that, in contrast to the traditional view of them being highly specialised, both martens and fishers are dietary generalists; however, they also appear to be specialists in complexity, at least in space and habitats. Collectively, martens and fishers exhibit high degrees of diet and habitat niche overlap across their ranges, and this overlap is likely to have the greatest fitness consequences for the smaller and subordinate martens. Nevertheless, fine‐scale habitat and prey partitioning, and especially partitioning along snow clines, seem to be the mechanisms by which these two taxa can coexist. We predict that rapid ecological change – especially from increasingly homogenised forests and prey communities, as well as from declining snow cover and snowpack due to climate warming – is likely to destabilise marten–fisher coexistence.
... We classified the impacts of each possible outcome as (1) positive (e.g., gaining novel adaptive variation), (2) neutral or unknown, (3) negative (e.g., extinction, loss of reproductive output) and (4) considered as negative. In this last category we included genetic swamping and introgression from a domesticated lineage, which are frequently described as negative in the literature [29,30,[65][66][67]. Given that direct empirical evidence for their negative effects is limited, we did not classify them as unequivocally negative outcomes. ...
... Nearly half (48%) of studies included in this systematic review that reported genetic swamping were focused on hybridization between domesticated mammals and their wild relatives, including wolf and domestic dog [38,81,135], wild boar and domestic pig [20,30,93] and wild cat and domestic cat [44]. More than a quarter (28%) of the studies reported genetic swamping of a native gene pool as the main result of hybridization between introduced species and native species, e.g., in Cervidae [36,136] and Mustelidae families [29,137,138]. Over 80% of the studies reporting genetic swamping focused on cases where hybridization was directly or indirectly caused by human actions, i.e., either domestication or species translocation (deliberate or unintentional). ...
Hybridization, defined as breeding between two distinct taxonomic units, can have an important effect on the evolutionary patterns in cross-breeding taxa. Although interspecific hybridization has frequently been considered as a maladaptive process, which threatens species genetic integrity and survival via genetic swamping and outbreeding depression, in some cases hybridization can introduce novel adaptive variation and increase fitness. Most studies to date focused on documenting hybridization events and analyzing their causes, while relatively little is known about the consequences of hybridization and its impact on the parental species. To address this knowledge gap, we conducted a systematic review of studies on hybridization in mammals published in 2010–2021, and identified 115 relevant studies. Of 13 categories of hybridization consequences described in these studies, the most common negative consequence (21% of studies) was genetic swamping and the most common positive consequence (8%) was the gain of novel adaptive variation. The total frequency of negative consequences (49%) was higher than positive (13%) and neutral (38%) consequences. These frequencies are biased by the detection possibilities of microsatellite loci, the most common genetic markers used in the papers assessed. As negative outcomes are typically easier to demonstrate than positive ones (e.g., extinction vs hybrid speciation), they may be over-represented in publications. Transition towards genomic studies involving both neutral and adaptive variation will provide a better insight into the real impacts of hybridization.
... Over the past several decades, surprising levels of phylogeographic structure in highly vagile carnivores in northern North America have been detected, including refugial signatures Colella et al. 2018b) and structure between mainland and Kenai Peninsula populations (wolves- Weckworth et al. 2005Weckworth et al. , 2011; brown bears- Morton et al. 2015). We provide a detailed examination of geographic structure in wolverines and the data are consistent with the isolation of the Kenai Peninsula wolverine population based on signals inferred from both the mitochondrial and nuclear genomes. ...
Cyclic climatic and glacial fluctuations of the Late Quaternary produced a dynamic biogeographic history for high latitudes. To refine our understanding of this history in northwestern North America, we explored geographic structure in a wide-ranging carnivore, the wolverine (Gulo gulo). We examined genetic variation in populations across mainland Alaska, coastal Southeast Alaska, and mainland western Canada using nuclear microsatellite genotypes and sequence data from the mitochondrial DNA (mtDNA) control region and Cytochrome b (Cytb) gene. Data from maternally inherited mtDNA reflect stable populations in Northwest Alaska, suggesting the region harbored wolverine populations since at least the Last Glacial Maximum (LGM; 21 Kya), consistent with their persistence in the fossil record of Beringia. Populations in Southeast Alaska are characterized by minimal divergence, with no genetic signature of long-term refugial persistence (consistent with the lack of pre-Holocene fossil records there). The Kenai Peninsula population exhibits mixed signatures depending on marker type: mtDNA data indicate stability (i.e., historical persistence) and include a private haplotype, whereas biparentally inherited microsatellites exhibit relatively low variation and a lack of private alleles consistent with a more recent Holocene colonization of the peninsula. Our genetic work is largely consistent with the early 20th century taxonomic hypothesis that wolverines on the Kenai Peninsula belong to a distinct subspecies. Our finding of significant genetic differentiation of wolverines inhabiting the Kenai Peninsula, coupled with the peninsula’s burgeoning human population and the wolverine’s known sensitivity to anthropogenic impacts, provides valuable foundational data that can be used to inform conservation and management prescriptions for wolverines inhabiting these landscapes.
... North American martens are relatively small meso-carnivores thought to be a single species until recently (Carr & Hicks, 1997;Colella, Johnson, & Cook, 2018;Colella, Wilson, Talbot, & Cook, 2018;Dawson et al., 2017). Now two species are hypothesized to have diverged in at least two independent glacial refugia south of North American ice sheets (Stone et al., 2002) In addition to natural hybrid zones, a series of intentional wildlife translocations in the mid-1900 s introduced M. americana to multiple NPC islands without prior knowledge of the native marten species in the region (Powell et al., 2012). ...
... Sequences were generated on an Illumina HiSeq X 10 through the Beijing Genomics Institute (BGI Americas, Philadelphia, PA, USA) and NextSeq 500 through the Molecular Biology Facility at the University of New Mexico. Sampling was based on previous single-and multi-locus genetic analyses (Colella, Wilson, et al., 2018;Dawson et al., 2017) that defined species limits and refined hybrid zone locations through the identification of mixed mitochondrial and nuclear haplotypes and morphological analyses (Colella, Johnson, et al., 2018). Liver tissue subsamples were loaned from the University of New Mexico's The Netherlands) protocol. ...
... Although unsampled in this study, Vancouver Island martens, subspecies M. c. vancouverensis (Grinnell & Dixon, 1926), are genetically aligned with M. caurina (Colella, Wilson, et al., 2018;Small et al., 2003) and the evolutionary history of this population may be key to interpreting the pre-glacial history of NPC martens. ...
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 D‐statistics (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, critical to interpreting refugial timing, duration, and community composition. Genomic reevaluations of other taxa along North America's North Pacific Coast may yield new and deeper perspectives on the history of refugial forest communities and the role of dynamic climate shifts in shaping high‐latitude diversity across complex insular landscapes.
... North American pine martens, Martes americana and M. caurina, are exemplar taxa with divergence dates currently estimated only from mitochondrial mutation rates. Colella et al. (2018b) estimated that divergence (speciation) of M. americana and M. caurina occurred between 18,843 kya (thousand years ago) and 9,260 kya using mutation rates derived from a closely related species, Mustela erminea (Hope et al. 2014). This places the divergence of these species at the end of the Wisconsin glaciation (80-11 kya) (Dyke 2004;Clark et al. 2009) and may support previous hypotheses that North American Martes underwent allopatric speciation during the late Pleistocene (126-11 kya) as a result of isolation within two glacial refugia, one in the eastern United States and the other in the western United States. ...
... To fill this knowledge gap, the congruence between the molecularly derived divergence age of M. americana and M. caurina (Colella et al. 2018b) and divergence dates calculated using fossil calibration points were examined. Gene sequences from four mitochondrial genes from specimens morphologically and/or genetically identified as M. americana and M. caurina from across their geographic ranges, including populations from the eastern U.S, which have historically been excluded from phylogenetic analyses of Martes Dawson and Cook 2012;Dawson et al. 2017), were collected and compared. ...
... hypothesized that the last common ancestor of M. americana and M. caurina came into North America via the Bering land bridge and then dispersed across North America during an interglacial period. Nucleotide substitution rates suggested these species diverged between 18,843 and 6,770 years ago, depending on the rate chosen (Colella et al. 2018b). This would place the speciation of M. americana and M. caurina at the end of the Wisconsin glaciation (11 kya) (Dyke 2004;Clark et al. 2009). ...
As molecularly derived phylogenies have become more prominent in determining evolutionary relationships, researchers have developed multiple methods of time-calibration to estimate ages of speciation or dispersal events. These methods, however, do not always arrive at congruent node ages. Fossil evidence is one of the most common forms of calibration for phylogenies, but age estimates can vary greatly depending on fossil choice, the taxa in question, and methodologies chosen. Using the North American pine martens, Martes americana and M. caurina, as exemplar taxa, previously calculated divergence dates derived from mutation rates and dates estimated using fossil-informed time-calibration are compared. Two fossil calibrated Bayesian phylogenies are generated: one constructed from cytochrome b; and another from a concatenated sequence matrix of 12S, 16S, cytochrome b, and Dloop. Both phylogenies are calibrated based on the fossil record of Martes at three nodes: divergence between ingroup and outgroup clades; node for crown M. americana; and node for crown M. caurina. Both phylogenies support the presence of two clades within Martes and estimate these clades, and thus species, diverged between 540 kya and 234 kya. This is approximately 200,000 years older than divergence ages calculated from mutation rates. The older dates generated here place Martes divergence within the Pre-Illinoan glacial episode instead of the younger Wisconsin glaciation as was previously hypothesized. The results of this study suggest that this clade likely evolved under the climatic influence of multiple glacial cycles throughout the Pleistocene.
... North American marten (Martes spp.) are a group for which genetic data are changing the understanding of how populations and lineages are structured across large landscapes (e.g., Colella et al., 2019) and provide an important example of how genetic data can inform wildlife management. Marten are actively harvested and managed throughout North America and may be sensitive to forest management (Kirk and Zielinski, 2009;Cushman et al., 2011;Moriarty et al., 2016), human recreation (Slauson et al., 2017), and climate change Wasserman et al., 2012a). ...
... Originally classified as two species -the American (Martes americana) and Pacific Coast (Martes caurina) marten (Merriam, 1890) -further morphometrics resulted in the assignment of M. caurina as a subspecies of M. americana (Wright, 1946). Although some authors continued to refer to two separate groups of marten in North America (Dawson and Cook, 2012), marten were subsequently considered, and managed, under the single species umbrella of M. americana (Colella et al., 2019). Recent molecular work has supported the original morphologically based two species classification of M. caurina and M. americana (Stone et al., 2002;Small et al., 2003;Dawson et al., 2017). ...
... Recent molecular work has supported the original morphologically based two species classification of M. caurina and M. americana (Stone et al., 2002;Small et al., 2003;Dawson et al., 2017). Analysis of widely spaced samples from western North America supports the longstanding notion (Wright, 1946) that there is a broad area of contact in the Inland Pacific Northwest including portions of British Columbia, Idaho, Montana, and Washington (Colella et al., 2019). ...
North American martens are forest dependent, influenced by human activity, and climate vulnerable. They have long been managed and harvested throughout their range as the American marten (Martes americana). Recent work has expanded evidence for the original description of two species in North America - M. americana and the Pacific Coast marten, M. caurina - but the geographic boundary between these groups has not been described in detail. From 2010 to 2016 we deployed 734 multi-taxa winter bait stations across a 53,474 km2 study area spanning seven mountain ranges within the anticipated contact zone along the border of Canada and the United States. We collected marten hair samples and developed genotypes for 15 polymorphic microsatellite loci for 235 individuals, and 493 base-pair sequences of the mtDNA gene COI for 175 of those individuals. Both nuclear and mitochondrial genetic structure identified a sharp break across the Clark Fork Valley, United States with M. americana and M. caurina occurring north and south of the break, respectively. We estimated global effective population size (N
e
) for each mountain range, clinal genetic neighborhood sizes (NS), calculated observed (H
o
) and expected (H
e
) heterozygosity, fixation index (F
ST
), and clinal measures of allelic richness (Ar), H
o
, and inbreeding coefficient (F
IS
). Despite substantial genetic structure, we detected hybridization along the fracture zone with both contemporary (nuclear DNA) and historic (mtDNA) gene flow. Marten populations in our study area are highly structured and the break across the fracture zone being the largest documented in North America (F
ST
range 0.21-0.34, mean = 0.27). With the exception of the Coeur d'Alene Mountains, marten were well distributed across higher elevation portions of our sampling area. Clinal NS values were variable suggesting substantial heterogeneity in marten density and movement. For both M. americana and M. caurina, elevationaly dependent gene flow and high genetic population structure suggest that connectivity corridors will be important to ensuring long-term population persistence. Our study is an example of how a combination of global and clinal molecular data analyses can provide important information for natural resource management.
... However, molecular genetic analyses support traditional morphological designation of martens (Merriam 1890;Clark et al. 1987) into the 2 distinct groups, americana and caurina (Dawson and Cook 2012;Colella et al. 2018). In fact, most molecular investigations demonstrate that mitochondrial DNA (mtDNA) divergence levels between americana and caurina are similar to those existing among the other 4 Palearctic Martes species with substantial nuclear allelic sorting between the 2 types, suggesting recognition as 2 distinct species (Carr and Hicks 1997;Dawson and Cook 2012;Colella et al. 2018Colella et al. , 2019. ...
The complex topography, climate, and geological history of Western North America have shaped contemporary patterns of biodiversity and species distributions in the region. Pacific martens (Martes caurina) are distributed along the northern Pacific Coast of North America with disjunct populations found throughout the Northwestern Forested Mountains and Marine West Coast Forest ecoregions of the West Coast. Martes in this region have been classified into subspecies; however, the subspecific designation has been extensively debated. In this study, we use genomic data to delineate conservation units of Pacific marten in the Sierra-Cascade-Coastal montane belt in the western United States. We analyzed the mitochondrial genome for 94 individuals to evaluate the spatial distribution and divergence times of major lineages. We further genotyped 401 individuals at 13 microsatellite loci to investigate major patterns of population structure. Both nuclear and mitochondrial DNA suggest substantial genetic substructure concordant with historical subspecies designations. Our results revealed that the region contains 2 distinct mitochondrial lineages: a Cascades/Sierra lineage that diverged from the Cascades/coastal lineage 2.23 (1.48-3.14 mya), consistent with orogeny of the Cascade Mountain chain. Interestingly, Pacific Martes share phylogeographic patterns similar with other sympatric taxa, suggesting that the complex geological history has shaped the biota of this region. The information is critical for conservation and management efforts, and further investigation of adaptive diversity is warranted following appropriate revision of conservation management designations.
... These fine-scale subpopulations are referred to as "local" sites in this study. We removed the subpopulation in VT-S from this analysis, as it was likely reintroduced from ME (Aylward et al. 2019), and translocations result in genetic patterns that are not indicative of natural processes (Colella et al. 2019). Furthermore, we removed any individual whose township locality could not be determined. ...
American marten (Martes americana) are a conservation priority in many forested regions of North America. Populations are fragmented at the southern edge of their distribution due to suboptimal habitat conditions. Facilitating gene flow may improve population resilience through genetic and demographic rescue. We used a multiscale approach to estimate the relationship between genetic connectivity and landscape characteristics among individuals at three scales in the northeastern United States: regional, subregional, and local. We integrated multiple modeling techniques and identified top models based on consensus. Top models were used to parameterize resistance surfaces at each scale, and circuit theory was used to identify potential movement corridors. Regional gene flow was affected by forest cover, elevation, developed land cover, and slope. At subregional and local scales, the effects were site specific and included subsets of temperature, elevation, developed land cover, and slope. Developed land cover significantly affected gene flow at each scale. At finer scales, lack of variance in forest cover may have limited the ability to detect a relationship with gene flow. The effect of slope on gene flow was positive or negative, depending on the site examined. Occupancy probability was a relatively poor predictor, and we caution its use as a proxy for landscape resistance. Our results underscore the importance of replication and multiscale approaches in landscape genetics. Climate warming and landscape conversion may reduce the genetic connectivity of marten populations in the northeastern United States, and represent the primary challenges to marten conservation at the southern periphery of their range.
... Intentional, informed genetic manipulations have the potential to overcome geographic impediments to gene flow by targeting the negative effects of inbreeding [118] in small populations. Genetic-rescue initiatives have proved occasionally successful [119] but are not reversible and should be employed judiciously due to potential swamping of local variation [115,120]. ...
Although logistically challenging to study, the Arctic is a bellwether for global change and is becoming a model for questions pertinent to the persistence of biodiversity. Disruption of Arctic ecosystems is accelerating, with impacts ranging from mixing of biotic communities to individual behavioral responses. Understanding these changes is crucial for conservation and sustainable economic development. Genomic approaches are providing transformative insights into biotic responses to environmental change, but have seen limited application in the Arctic due to a series of limitations. To meet the promise of genome analyses, we urge rigorous development of biorepositories from high latitudes to provide essential libraries to improve the conservation, monitoring, and management of Arctic ecosystems through genomic approaches.
