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). ...
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). ...
Urbanisation is rapidly transforming terrestrial environments, especially in the tropics. Many squirrel species tolerate urbanisation, but studies are biased towards temperate regions. We quantify the distribution and abundance of squirrels and (ecologically similar) tree-shrews along an urbanisation gradient in a rapidly urban-ising tropical mega-city (Bangkok, Thailand) located within the Indo-Burma biodiversity hotspot. We used repeated point counts in 150 1 km cells, selected using random stratification across the urbanisation gradient. We quantified species responses to (i) urbanisation intensity (measured using impervious surface cover), (ii) environmental conditions (woodland quantity and quality, human disturbance and predation pressure from free-ranging cats and dogs) and (iii) urbanisation impacts on hybridisation between congeneric Callosciurus squirrels. Three of the six species from the regional species pool were extremely rare or absent within our study region (Tamiops macclellandi, Callosciurus caniceps and Menetes berd-morei). Of the three more widespread species (Tupaia belangeri, Callosciurus fin-laysonii and Callosciurus erythraeus) only C. finlaysonii had a higher abundance in more urban locations. The increasing intensity of urbanisation has thus markedly reduced squirrel diversity and abundance, contrasting with the perception from temperate regions that squirrels typically tolerate urbanisation. Urbanisation is thus likely to have reduced important ecological functions provided by squirrels, such as seed dispersal. Models of species responses to environmental conditions suggest that improving habitat quality by increasing tree cover and diversity at local and landscape scales and reducing human disturbance and numbers of feral dogs would partially mitigating adverse impacts of urbanisation on tropical squirrels and tree-shrews. Urban infrastructure (bridge construction across the Chao-Praya River) appears to have increased the permeability of a geographic barrier that previously separated C. finlaysonii and C. erythraeus distributions, increasing hybridisation rates. Our study enhances understanding of the ecological impacts of urbanisation in biodiverse tropical regions and the action required to mitigate these impacts.
... 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 . 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. ...
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 . Hybridization and resulting admixture represent another confounding factor when taxa are identified based on phenotype . In our study, genotypes of two samples reflected admixture, and both were from a SAFE site (Saybrook) with a preponderance of M. pennsylvanicus. ...
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 ). ...
Introductions of non-native lineages increase opportunities for hybridization. Non-native lineages of the common wall lizard, Podarcis muralis, are frequently introduced in cities where they hybridize with native populations. We aimed at unravelling the invasion history and admixture of native and non-native wall lizards in four German cities using citywide, comprehensive sampling. We barcoded and genotyped 826 lizards and tested if gene flow in populations composed of admixed native and introduced lineages is facilitated by similar environmental factors to those in native populations by comparing fine-scale landscape genetic patterns. In cities with non-native lineages, lizards commonly occurred in numerous clusters of hybrid swarms, which showed variable lineage composition, consisting of up to four distinct evolutionary lineages. Hybrid swarms held vast genetic diversity and showed recent admixture with other hybrid swarms. Landscape genetic analyses showed differential effects of cityscape structures across cities, but identified water bodies as strong barriers to gene flow in both native and admixed populations. By contrast, railway tracks facilitated gene flow of admixed populations only. Our study shows that cities represent unique settings for hybridization, caused by multiple introductions of non-native taxa. Cityscape structure and invasion histories of cities will determine future evolutionary pathways at these novel hybrid zones.
In Canada, subspecies of the yellow-pine chipmunk (Neotamias amoenus luteiventris) and red-tailed chipmunk (Neotamias ruficaudus ruficaudus) co-occur in a small area of the Rocky Mountains in southwestern Alberta and southeastern British Columbia. Some N. a. luteiventris individuals in this area are of hybrid ancestry, carrying a mitochondrial DNA gene of N. r. ruficaudus. We tested for phenotypic hybridization by comparing genital bone morphology, body size, cranial mandibular morphology, and tail color of mitochondrial hybrids with specimens of the 2 parental reference groups identified from genetics or genital morphology. Hybrids were indistinguishable from the N. a. luteiventris reference group, demonstrating no intermediacy or increased variability. Our results are consistent with genetic data that suggest minimal nuclear gene flow between the 2 taxa. Five hybrid locations were within the contact zone, but 6 were 1498 km beyond the known range extent of N. r. ruficaudus. These peripheral occurrences may be a legacy of a past range decline of N. r. ruficaudus in response to Holocene climatic changes that left hybrids outside the present-day contact zone. We recommend more field research in the Canadian Rocky Mountains to determine the full range extent of N. r. ruficaudus and N. a. luteiventris of hybrid ancestry.
Although naturally heterogeneous environments can lead to mosaic hybrid zones, human-induced habitat fragmentation can also lead to environmental heterogeneity and hybridization. Here we quantify phenotypic and molecular divergence across a reed frog mosaic hybrid zone on São Tomé Island as a first step towards understanding the consequences of hybridization across this heterogeneous landscape. The São Tomé giant reed frog (Hyperolius thomensis) is strongly tied to cool, wet, forest habitats whereas the distribution of Moller’s reed frog (H. molleri) spans cool, wet, forests to warm, dry, disturbed habitats. Correspondingly, hybridization is concentrated in the more forested, cool, wet sites relative to non-forested, warmer, drier habitats. Four of six sites with hybrid frogs are artificial water bodies near the forest edge, indicating that both breeding habitat and broader scale environmental variation are probably important for understanding interspecific interactions and the extent of hybridization in this system. Phenotypic variation (body size and ventral coloration) largely tracks genetic and environmental variation across the hybrid zone with larger and more pigmented frogs occurring in forested, cool, wet habitats. Understanding whether human-induced changes in habitat break down reproductive barriers will be essential for conservation management of the less abundant, forest-associated H. thomensis in the face of rampant hybridization.
We analyzed the use of habitat terminology in articles from the Journal of Wildlife Management (JWM) each year (1998–2017) in course descriptions from 1 wildlife biology degree program in each state within the United States, and by wildlife‐related non‐profit organizations and state and federal agencies. Sixty‐five percent of JWM articles fluctuated in their correct use and 31% incorrectly used the term habitat and there was no significant decrease in the misuse of the term since 1998. Habitat type was used in 46% of the papers analyzed and was always used incorrectly. Misuse of the term habitat type in JWM articles decreased since 1998, from 70% of articles using the term from 1998 to 2002, 50% from 2013 to 2016, and no papers using the term in 2017. From the course descriptions using the term habitat, 75% fluctuated in their correct use and 13% incorrectly used habitat terminology. When considering only the management course descriptions and the term wildlife habitat as correct, 28% of programs fluctuated in their correct use and 31% incorrectly used habitat terminology. All wildlife‐related organizations fluctuated in their correct use of the term habitat. Our results demonstrate that the misuse of habitat terminology is still being missed during the JWM editorial process, at least until very recently. In combination with the continued misuse of habitat terminology in the primary literature, our results suggest an underlying reason for the continued incorrect use of habitat terminology is the misuse of the terms by educators within wildlife degree programs and by wildlife‐related organizations. By dealing with misuse of habitat terminology at the undergraduate level concurrent with misuse in the primary literature and by wildlife‐related organizations, we should begin to see a shift in the correct use of habitat terminology in current and future generations of natural resource professionals.
Hybridization between naturally co-occurring species that normally do not interbreed is being documented following anthropogenic habitat modifications for an increasing number of taxa. Here, we evaluate the mechanisms by which disturbance promotes hybridization and highlight the utility of human-caused hybridization for understanding evolution. Monitoring hybridization dynamics before, and following, disturbance over multiple timescales offers a unique opportunity to understand how disturbances alter species interactions and to pinpoint the mechanisms that cause species barriers to fail. Identifying the conditions promoting hybridization in disturbed habitats, the generality of these conditions across taxa, and the taxa most affected by human-mediated change is critical for furthering our understanding of human impacts on evolution and for informing management.
The ecology of a species strongly influences genetic variation and population structure. This interaction has important conservation implications because taxa with low dispersal capability and inability to use different habitats are more susceptible to anthropogenic stressors. Ocelots (Leopardus pardalis
albescens) and bobcats (Lynx rufus texensis) are sympatric in Texas and northeastern Mexico; however, their ecology and conservation status are markedly different. We used 10 microsatellite loci and a 397-bp segment of the mitochondrial control region to examine how historical and ecological differences in these two species have influenced current patterns of genetic diversity in a landscape heavily altered by anthropogenic activities. Substantially higher genetic diversity (heterozygosity and haplotype diversity) and population connectivity was observed for bobcats in comparison to ocelots. The level of divergence among proximate ocelot populations (<30 km) was greater than between bobcat populations separated by >100 km. Ocelot populations in the US have never recovered from reductions experienced during the twentieth century, and their low genetic variation and substantial isolation are exacerbated by strong preference for dense native thornshrub and avoidance of open habitat. In contrast, despite continued legal harvesting and frequent road-related mortality, bobcats have maintained wide distribution, high abundance, and population connectivity. Our study illustrates that sympatric species with a similar niche can still have sufficient ecological differences to alter their response to anthropogenic change. Sensitive species, such as the ocelot, require additional conservation actions to sustain populations. Ecological differences among species occupying a similar guild are important to consider when developing conservation plans.
We describe a model-based clustering method for using multilocus genotype data to infer population structure and assign individuals to populations. We assume a model in which there are K populations (where K may be unknown), each of which is characterized by a set of allele frequencies at each locus. Individuals in the sample are assigned (probabilistically) to populations, or jointly to two or more populations if their genotypes indicate that they are admixed. Our model does not assume a particular mutation process, and it can be applied to most of the commonly used genetic markers, provided that they are not closely linked. Applications of our method include demonstrating the presence of population structure, assigning individuals to populations, studying hybrid zones, and identifying migrants and admixed individuals. We show that the method can produce highly accurate assignments using modest numbers of loci—e.g., seven microsatellite loci in an example using genotype data from an endangered bird species. The software used for this article is available from http://www.stats.ox.ac.uk/~pritch/home.html.
Interest in, and opportunities to include functional and phylogenetic attributes of species in community ecology and biogeography are rapidly growing and seen as vital for the assessment of status and trends in biodiversity. However, the fundamental underlying evidence remains the (co-)occurrence of the biological units, such as species, in time and space and our ability to appropriately detect and quantify them. Here, we examine the implications of imperfect detection of species for functional and phylogenetic diversity (FD and PD) estimates. We explore how FD and PD might have different detectabilities than taxonomic diversity (TD) and how all three might vary differently along spatial and environmental gradients. We also extend occupancy modeling and dendrogram-based methods to address the imperfect detection of different biodiversity facets.
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.