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Landscape disturbance and sporadic hybridization complicate field identification of chipmunks: Chipmunk Genetic Identification

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Chipmunks (Tamias spp.) in western North America are important for their numerical abundance, their role in pathogen transmission, and the composition and structure of food webs. As such, land management agencies (e.g., U.S. Forest Service) often conduct field surveys to monitor the diversity and abundance of chipmunk species as a measure of forest health. These small mammal communities often include several morphologically similar chipmunk species, some of which occasionally hybridize, which can make field identification of species difficult. However, species-specific differences in both spatial distribution and habitat use make it imperative that biotic inventories correctly identify chipmunk species. We compared molecular-based and field-based, external phenotypic identifications of 4 chipmunk species in the Lake Tahoe Basin of the Sierra Nevada in California and Nevada, USA. Across all years and sites, we found an error rate of 14% for field-based identifications with significantly lower rates of misidentification in relatively undisturbed wildlands in comparison to recently burned wildlands or urbanized sites. We also found evidence for sporadic hybridization between focal species, including cases of mito-nuclear mismatch. Our study highlights the utility of molecular tools in corroborating field identifications of chipmunks in changing landscapes.
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... Revealing ancient hybridization in different taxa also broadens understanding of the contribution of hybridization to mammalian evolution (e.g., Marques et al., 2017). In the ground squirrels Marmotini up to a quarter of species are involved in hybridization events of varying intensity, from sporadic hybridization to the formation of hybrid zones and wide introgression according to our estimates of the literature data (Semenova, 1967;Nikol'skii et al., 1983;Smirin et al., 1985;Good et al., 2008;Stangl et al., 2012;Thompson et al., 2013;Ermakov et al., 2015;Frare et al., 2017;Ivanova et al., 2017;Leitner et al., 2017;Kapustina et al., 2018). ...
... The level of hybridization we documented between M. baibacina and M. sibirica is lower than what has been reported in Palaearctic Spermophilus, both in the proportion of hybrids in populations and in spatial coverage (Ermakov et al., 2002(Ermakov et al., , 2015Titov et al., 2005;Spiridonova et al., 2006;Ivanova et al., 2017). But in general, hybridization occurs more frequently in secondary contact zones within Palaearctic Marmota and Spermophilus than Nearctic Marmotini (Hird et al., 2010;Stangl et al., 2012;Frare et al., 2017;Leitner et al., 2017). This may be due to the greater divergence of Nearctic species and, consequently, forming more effective interspecific barriers compared with Palearctic species (Herron et al., 2004;Brandler et al., 2010a). ...
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The role of hybridization as one of the factors of speciation in mammals has been underestimated for a long time, but now there is a lot of data on its impact in mammalian evolution. Hybridization of species often occurs in their secondary contact zones, which is a natural model for testing factors that ensure species integrity. Studies of hybrid zones are increasingly revealing the essential role of ecological and behavioral features both in initiating crossbreeding and in maintaining interspecific barriers. We studied the hybridization of two species of marmots Marmota baibacina and M. sibirica in the zone of sympatry in Mongolian Altai Mountains. We used a bioacoustic approach to determine the localization of individuals of different species and their cohabitation sites. Genetic typing with two diploid nuclear markers and one marker each of paternal and maternal lines was used to identify hybrids. Habitat preferences of marmots were studied to understand the conditions for the formation of heterospecific pairs. We found a high proportion of hybrid individuals in boulder screes where conditions for the formation of heterospecific pairs probably exist. Our data indicate the viability and fertility of F1 hybrids and their descendants. We hypothesize that the environmental preferences and behavioral features of both species of marmots are important factors that both create conditions for hybridization and limit hybrid dispersal.
... It is also plausible that urbanisation could reduce hybridisation rates by limiting the population densities of one or more parental species. Relatively little research has assessed how urbanisation influences hybridisation although those studies that have been conducted to date have found increased hybridisation rates in a number of vertebrate groups including fish (Heath, Bettles & Roff, 2010), reptiles (Haines et al., 2016), and mammals (Frare et al., 2017). ...
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... The presence of admixed individuals with intermediate phenotypes may impede species identification in the field. For instance, field identification of four chipmunk species (Tamias spp.) in the Sierra Nevada, USA, was associated with 14% error rate, which was in part attributed to sporadic hybridization among these species [190]. The fitness consequences of intermediate phenotypic traits have rarely been studied and therefore this outcome of hybridization could not be classified as either positive or negative. ...
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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.
... Similar disparities have been observed in other studies [31]. Hybridization and resulting admixture represent another confounding factor when taxa are identified based on phenotype [64]. In our study, genotypes of two samples reflected admixture, and both were from a SAFE site (Saybrook) with a preponderance of M. pennsylvanicus. ...
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Ecological restoration can promote biodiversity conservation in anthropogenically fragmented habitats, but effectiveness of these management efforts need to be statistically validated to determine 'success.' One such approach is to gauge the extent of recolonization as a measure of landscape permeability and, in turn, population connectivity. In this context, we estimated dispersal and population connectivity in prairie vole (Microtus ochrogaster; N = 231) and meadow vole (M. pennsylvanicus; N = 83) within five tall-grass prairie restoration sites embedded within the agricultural matrix of midwestern North America. We predicted that vole dispersal would be constrained by the extent of agricultural land surrounding restored habitat patches, spatially isolating vole populations and resulting in significant genetic structure. We first employed genetic assignment tests based on 15 microsatellite DNA loci to validate field-derived species-designations, then tested reclassified samples with multivariate and Bayesian clustering to assay for spatial and temporal genetic structure. Population connectivity was further evaluated by calculating pairwise F ST , then potential demographic effects explored by computing migration rates, effective population size (N e), and average relatedness (r). Genetic species assignments reclassified 25% of initial field identifications (N = 11 M. ochrogaster; N = 67 M. pennsylvanicus). In M. ochrogaster population connectivity was high across the study area, reflected in little to no spatial or temporal genetic structure. In M. pennsylvanicus genetic structure was detected, but relatedness estimates identified it as kin-clustering instead, underscoring social behavior among populations rather than spatial isolation as the cause. Estimates of N e and r were stable across years, reflecting high dispersal and demographic resilience. Combined, these metrics suggest the agricultural matrix is highly permeable for voles and does not impede dispersal. High connectivity observed confirms that the restored landscape is productive and PLOS ONE PLOS ONE | https://doi.org/10.1371/journal.pone.
... Therefore, they are interesting systems for the study of evolutionary trajectories. However, despite the importance of urban areas for novel species interactions, hybridization has so far rarely been studied in cities (but see a study on chipmunks [43]). ...
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The chipmunks are a Holarctic group of ground squirrels currently allocated to the genus Tamias within the tribe Marmotini (Rodentia: Sciuridae). Cranial, post-cranial, and genital morphology, cytogenetics, and genetics each separate them into three distinctive and monophyletic lineages now treated as subgenera. These groups are found in eastern North America, western North America, and Asia, respectively. However, available genetic data (mainly from mitochondrial cytochrome b) demonstrate that the chipmunk lineages diverged early in the evolution of the Marmotini, well before various widely accepted genera of marmotine ground squirrels. Comparisons of genetic distances also indicate that the chipmunk lineages are as or more distinctive from one another as are most ground squirrel genera. Chipmunk fossils were present in the late Oligocene of North America and shortly afterwards in Asia, prior to the main radiation of Holarctic ground squirrels. Because they are coordinate in morphological, genetic, and chronologic terms with ground squirrel genera, the three chipmunk lineages should be recognized as three distinct genera, namely, Tamias Illiger, 1811, Eutamias Trouessart, 1880, and Neotamias A. H. Howell, 1929. Each is unambiguously diagnosable on the basis of cranial, post-cranial, and external morphology.