Habitat distribution influences dispersal and fine-scale genetic population structure of eastern foxsnakes (Mintonius gloydi) across a fragmented landscape

Dispersal is a fundamental attribute of species in nature and shapes population dynamics, evolutionary trajectories and genetic variation across spatial and temporal scales. It is increasingly clear that landscape features have large impacts on dispersal patterns. Thus, understanding how individuals and species move through landscapes is essential for predicting impacts of landscape alterations. Information on dispersal patterns, however, is lacking for many taxa, particularly reptiles. Eastern foxsnakes (Mintoinus gloydi) are marsh and prairie specialists that avoid agricultural fields, but they have persisted across a fragmented region in southwestern Ontario and northern Ohio. Here, we combined habitat suitability modelling with population genetic analyses to infer how foxsnakes disperse through a habitat mosaic of natural and altered landscape features. Boundary regions between the eight genetic clusters, identified through assignment tests, were comprised of low suitability habitat (e.g. agricultural fields). Island populations were grouped into a single genetic cluster, and comparatively low F(ST) values between island and mainland populations suggest open water presents less of a barrier than nonsuitable terrestrial habitat. Isolation by resistance and least-cost path analysis produced similar results with matrices of pairwise individual genetic distance significantly more correlated to matrices of resistance values derived from habitat suitability than models with an undifferentiated landscape. Spatial autocorrelation results matched better with assignment results when incorporating resistance values rather than straight-line distances. All analyses used in our study produced similar results suggesting that habitat degradation limits dispersal for foxsnakes, which has had a strong effect on the genetic population structure across this region.     

Patterns of genetic differentiation in Thamnophis and Taricha from the Pacific Northwest

Aim The co‐evolutionary interaction between the common garter snake, Thamnophis sirtalis, and the rough‐skinned newt, Taricha granulosa, takes place throughout much of the Pacific Northwest (North America). The biogeography of the Pacific Northwest has been heavily influenced by the last Pleistocene glaciation, which reached a maximum as late as 14,000 yr bp . We researched: (1) what type of population structure is present for garter snakes and newts, (2) whether the population structure of these species is consistent with a Pleistocene glaciation hypothesis, and (3) how population structure and migration possibly affect co‐evolution between these species. Location The Pacific Northwest of North America, specifically northern California, Oregon and Washington in the USA. Methods We sampled approximately 20 populations for each species from three different transects. Using microsatellite markers and tissue samples from both species, we quantified the population structure for both species. Individual‐based assignment tests were used to estimate contemporary migration rates. Results Both Th. sirtalis and Ta. granulosa exhibited little genetic differentiation among our study sites, even among those separated by large distances. Significant population structure was detected on multiple geographic scales. Differences in population structure were observed among transects and between garter snake and newt transects. Contemporary migration rate estimates indicate high levels of genetic exchange between populations. Main conclusions Prior to this study, little was known about the fine‐scale population structure of either species in this region. Patterns of population structure for garter snakes and newts reflect a shared biogeographical history affected by the Pleistocene glaciation in the Pacific Northwest. Both species apparently migrate frequently between populations, thus potentially retarding the process of adaptive co‐evolution. We find that populations from a northern coastal transect (Washington) are most likely to be locally adapted.     

Population genetic analysis identifies source-sink dynamics for two sympatric garter snake species (Thamnophis elegans and Thamnophis sirtalis)

Population genetic structure can be shaped by multiple ecological and evolutionary factors, but the genetic consequences of these factors for multiple species inhabiting the same environment remain unexplored. We used microsatellite markers to examine the population structures of two coexisting species of garter snake, Thamnophis elegans and Thamnophis sirtalis, to determine if shared landscape and biology imposed similar population genetic structures. These snakes inhabit a series of ponds, lakes and flooded meadows in northern California and tend to converge on prey type wherever they coexist. Both garter snakes had comparable effective population sizes and bidirectional migration rates (estimated using a maximum-likelihood method based on the coalescent) with low but significant levels of genetic differentiation (F(ST) = 0.024 for T. elegans and 0.035 for T. sirtalis). Asymmetrical gene flow revealed large source populations for both species as well as potential sinks, suggesting frequent extinction-recolonization and metapopulation dynamics. In addition, we found a significant correlation between their genetic structures based on both pairwise F(ST)s for shared populations (P = 0.009) and for bidirectional migration rates (P = 0.024). Possible ecological and evolutionary factors influencing similarities and differences in genetic structure for the two species are discussed. Genetic measures of effective population size and migration rates obtained in this study are also compared with estimates obtained from mark-recapture data.     

An Examination of Scale-Dependent Resource Use by Eastern Hognose Snakes in Southcentral New Hampshire

ABSTRACT The decline of many snake populations is attributable to habitat loss, and knowledge of habitat use is critical to their conservation. Resource characteristics (e.g., relative availability of different habitat types, soils, and slopes) within a landscape are scale-dependent and may not be equal across multiple spatial scales. Thus, it is important to identify the relevant spatial scales at which resource selection occurs. We conducted a radiotelemetry study of eastern hognose snake (Heterodon platirhinos) home range size and resource use at different hierarchical spatial scales. We present the results for 8 snakes radiotracked during a 2-year study at New Boston Air Force Station (NBAFS) in southern New Hampshire, USA, where the species is listed by the state as endangered. Mean home range size (minimum convex polygon) at NBAFS (51.7 ± 14.7 ha) was similar to that reported in other parts of the species’ range. Radiotracked snakes exhibited different patterns of resource use at different spatial scales. At the landscape scale (selection of locations within the landscape), snakes overutilized old-field and forest edge habitats and underutilized forested habitats and wetlands relative to availability. At this scale, snakes also overutilized areas containing sandy loam soils and areas with lower slope (mean slope = 5.2% at snake locations vs. 6.7% at random locations). We failed to detect some of these patterns of resource use at the home range scale (i.e., within the home range). Our ability to detect resource selection by the snakes only at the landscape scale is likely the result of greater heterogeneity in macrohabitat features at the broader landscape scale. From a management perspective, future studies of habitat selection for rare species should include measurement of available habitat at spatial scales larger than the home range. We suggest that the maintenance of open early successional habitats as a component of forested landscapes will be critical for the persistence of eastern hognose snake populations in the northeastern United States.     

Geographic variation in timekeeping systems among three populations of garter snakes (Thamnophis sirtalis) in a common garden

Transduction of environmental cues into endocrine signals that synchronize physiology and behavior with optimal environmental conditions is central to an animal's timekeeping system. Using a common garden approach, we investigated possible geographic variation in timekeeping systems by comparing 24-h melatonin and corticosterone rhythms and reproductive behavior among three populations of garter snakes with very different life histories: red-sided garter snakes (Thamnophis sirtalis parietalis) from Manitoba, Canada; red-spotted garter snakes (Thamnophis sirtalis concinnus) from western Oregon; and eastern garter snakes (Thamnophis sirtalis sirtalis) from southern Florida. Melatonin and corticosterone cycles differed significantly among the three snake populations in a majority of the sampling periods. Population differences were observed across a wide range of acclimatization conditions and were themselves plastic (i.e., one snake population was not consistently different from the others). Changes in courtship behavior during emergence also varied significantly among populations. Our data support the hypothesis that endogenous timekeeping systems have evolved in the presence of unique environmental conditions. Further research is necessary to determine whether this geographic variation results from inherent genetic differences or whether it is a product of development. These studies provide insight into the evolution of timekeeping systems and may aid in understanding the potential effects of environmental perturbations on seasonal physiology and behavior.     

Approximate Bayesian computation reveals the factors that influence genetic diversity and population structure of foxsnakes

Contemporary geographical range and patterns of genetic diversity within species reflect complex interactions between multiple factors acting across spatial and temporal scales, and it is notoriously difficult to disentangle causation. Here, we quantify patterns of genetic diversity and genetic population structure using mitochondrial DNA sequences (101 individuals, cytochrome b) and microsatellites (816 individuals, 12 loci) and use Approximate Bayesian computation methods to test competing models of the demographic history of eastern and western foxsnakes. Our analyses indicate that post-glacial colonization and past population declines, probably caused by the infilling of deciduous forest and cooler temperatures since the mid-Holocene, largely underpin large-scale genetic patterns for foxsnakes. At finer geographical scales, our results point to more recent anthropogenic habitat loss as having accentuated genetic population structure by causing further declines and fragmentation.     

Microsatellite markers developed from Thamnophis elegans and Thamnophis sirtalis and their utility in three species of garter snakes

Previous studies of polyandry and population genetics in garter snakes have been hampered by the limited number of available microsatellite markers. Here we report another six dinucleotide microsatellite markers, doubling the number of previously available loci. The majority of the loci exhibit utility across a broad geographical range for the common garter snake and also cross‐amplify effectively in samples from two other Thamnophis species.     

Species specificity of methyl ketone profiles in the skin lipids of female garter snakes,genus Thamnophis

One of the relatively few vertebrate pheromones to be chemically identified, the female sex pheromone of the red-sided garter snake (Thamnophis sirtalis parietalis) is a series of saturated and monounsaturated methyl ketones contained within female skin lipids. During the breeding season, this pheromone is responsible for eliciting male courtship behaviors and males are able to utilize pheromonal variation to discriminate among females. While the pheromone system of the red-sided garter snake has been the subject of many studies, relatively little is known about the pheromone systems of other garter snakes. Through chemical analyses, we demonstrate that female skin lipids of the red-spotted garter snake (Thamnophis sirtalis concinnus), northwestern garter snake (Thamnophis ordinoides), and plains garter snake (Thamnophis radix) contain similar methyl ketones. The methyl ketone profiles of these snakes differ qualitatively from one another and from the methyl ketone profiles of red-sided garter snakes with differences particularly pronounced between sympatric species. Our results provide evidence that the use of methyl ketones in sexual signaling may be ubiquitous for Thamnophis species and suggest that these compounds could play a role in reproductive isolation between species in this genus.     

Ecological correlates of population genetic structure: a comparative approach using a vertebrate metacommunity

Identifying ecological factors associated with population genetic differentiation is important for understanding microevolutionary processes and guiding the management of threatened populations. We identified ecological correlates of several population genetic parameters for three interacting species (two garter snakes and an anuran) that occupy a common landscape. Using multiple regression analysis, we found that species interactions were more important in explaining variation in population genetic parameters than habitat and nearest-neighbour characteristics. Effective population size was best explained by census size, while migration was associated with differences in species abundance. In contrast, genetic distance was poorly explained by the ecological correlates that we tested, but geographical distance was prominent in models for all species. We found substantially different population dynamics for the prey species relative to the two predators, characterized by larger effective sizes, lower gene flow and a state of migration-drift equilibrium. We also identified an escarpment formed by a series of block faults that serves as a barrier to dispersal for the predators. Our results suggest that successful landscape-level management should incorporate genetic and ecological data for all relevant species, because even closely associated species can exhibit very different population genetic dynamics on the same landscape.     

Landscape genetics of an endangered salt marsh endemic: Identifying population continuity and barriers to dispersal

Preserving the genetic diversity of endangered species is fundamental to their conservation and requires an understanding of genetic structure. In turn, identification of landscape features that impede gene flow can facilitate management to mitigate such obstacles and help with identifying isolated populations. We conducted a landscape genetic study of the endangered salt marsh harvest mouse (Reithrodontomys raviventris), a species endemic to the coastal marshes of the San Francisco Estuary of California. We collected and genotyped?>?500 samples from across the marshes of Suisun Bay which contain the largest remaining tracts of habitat for the species. Cluster analyses and a population tree identified three geographically discrete populations. Next, we conducted landscape genetic analyses at two scales (the entire study area and across the Northern Marshes) where we tested 65 univariate models of landscape features and used the best supported to test multivariable analyses. Our analysis of the entire study area indicated that open water and elevation (>?2 m) constrained gene flow. Analysis of the Northern Marshes, where low elevation marsh habitat is more continuous, indicated that geographic distance was the only significant predictor of genetic distance at this scale. The identification of a large, connected population across Northern Marshes achieves a number of recovery targets for this stronghold of the species. The identification of landscape features that act as barriers to dispersal enables the identification of isolated and vulnerable populations more broadly across the species range, thus aiding conservation prioritization.

     

Effects of population size and isolation on the genetic structure of the East African mountain white‐eye Zosterops poliogaster (Aves)

Habitat size, quality and isolation determine the genetic structure and diversity of populations and may influence their evolutionary potential and vulnerability to stochastic events. Small and isolated populations are subject to strong genetic drift and can lose much of their genetic diversity due to stochastic fixation and loss of alleles. The mountain white‐eye Zosterops poliogaster, a cloud forest bird species, is exclusively found in the high mountains of East Africa. We analysed 13 polymorphic microsatellites for 213 individuals of this species that were sampled at different points in time in three mountain massifs differing in habitat size, isolation and habitat degradation. We analysed the genetic differentiation among mountain populations and estimated the effective population sizes. Our results indicate three mountain‐specific genetic clusters. Time cohorts did not show genetic divergences, suggesting that populations are large enough to prevent strong drift effects. Effective population sizes were higher in larger and geographically interconnected habitat patches. Our findings underline the relevance of ecological barriers even for mobile species and show the importance of investigating different estimators of population size, including both approaches based on single and multiple time‐points of sampling, for the inference of the demographic status of a population. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 828–836.     

Systematics of the Eimerian Parasites from North American Snakes of the Family Colubridae,and their Prevalence in the Colubrids of Iowa*

A survey of 117 Iowa snakes, representing 18 species within 12 genera, revealed the presence of 6 species of Eimeria, 5 of which are described as new and 1 of which (E. zamenis) is redescribed. Those species found, the average length-width dimensions of their oocysts ( in micrometers ), and the respective hosts from which they were isolated were as follows: E. attenuata sp. n., 22.2 × 12.6, from 1 of 25 red-sided garter snakes [Thamnophis sirtalis parietalis (Say)] and 1 of 14 northern water snakes [Natrix sipedon sipedon (Linnaeus)]; E. iowaensis sp. n., 17.8 × 14.5, from 1 of 25 redsided garter snakes; E. hydrophis sp. n., 15.4 × 10.9, from 5 of 14 northern water snakes and 1 of 1 diamond-backed water snake [N. rhombifera rhombifera (Hallowell)]; E. helmisophis sp. n., 13.8 × 10.6, from 1 of 5 western worm snakes [Carphophis amoenus vermis (Kennicott)]; E. collanuli sp. n., 33.1 × 18.3, from 1 of 14 prairie ring-neck snakes (Diadophis punctatus arnyi Kennicott), and E. zamenis, 31.0 × 17.0, from 1 of 6 eastern yellow-bellied racers (Coluber constrictor flaviventris Say) and 1 of 1 eastern milk snake [Lampropeltis triangulum triangulum (Lacépède)]. The overall infection rate for the 117 snakes examined was 9.2%; these data are tabulated. In addition, the possible synonymy of E. lampropeltis with E. zamenis is considered, and the probable status of E. attenuata, E. hydrophis, E. zamenis, and E. annea, as parasites of multiple host species, is reviewed with regard to the phylogenetic relationships of the respective hosts from which they have been reported.     

Conservation genetics of the yellow-bellied toad (Bombina variegata): population structure,genetic diversity and landscape effects in an endangered amphibian

Revealing patterns of genetic diversity and barriers for gene flow are key points for successful conservation in endangered species. Methods based on molecular markers are also often used to delineate conservation units such as evolutionary significant units and management units. Here we combine phylo-geographic analyses (based on mtDNA) with population and landscape genetic analyses (based on microsatellites) for the endangered yellow-bellied toad Bombina variegata over a wide distribution range in Germany. Our analyses show that two genetic clusters are present in the study area, a northern and a southern/central one, but that these clusters are not deeply divergent. The genetic data suggest high fragmentation among toad occurrences and consequently low genetic diversity. Genetic diversity and genetic connectivity showed a negative relationship with road densities and urban areas surrounding toad occurrences, indicating that these landscape features act as barriers to gene flow. To preserve a maximum of genetic diversity, we recommend considering both genetic clusters as management units, and to increase gene flow among toad occurrences with the aim of restoring and protecting functional meta-populations within each of the clusters. Several isolated populations with especially low genetic diversity and signs of inbreeding need particular short-term conservation attention to avoid extinction. We also recommend to allow natural gene flow between both clusters but not to use individuals from one cluster for translocation or reintroduction into the other. Our results underscore the utility of molecular tools for species conservation, highlight outcomes of habitat fragmentation onto the genetic structure of an endangered amphibian and reveal particularly threatened populations in need for urgent conservation efforts.

     

Similarity of contemporary and historical gene flow among highly fragmented populations of an endangered rattlesnake

Populations of endangered taxa in recently fragmented habitats often show high levels of genetic structure, but the role that contemporary versus historical processes play in generating this pattern is unclear. The eastern massasauga rattlesnake (Sistrurus c. catenatus) is an endangered snake that presently occurs throughout central and eastern North America in a series of populations that are isolated because of habitat fragmentation and destruction. Here, we use data from 19 species-specific microsatellite DNA loci to assess the levels of genetic differentiation, genetic effective population size, and contemporary and historical levels of gene flow for 19 populations sampled across the range of this snake. Eastern massasaugas display high levels of genetic differentiation (overall θ(Fst) = 0.21) and a Bayesian clustering method indicates that each population represents a unique genetic cluster even at regional spatial scales. There is a twofold variation in genetically effective population sizes but little genetic evidence that populations have undergone recent or historical declines in size. Finally, both contemporary and historical migration rates among populations were low and similar in magnitude even for populations located <7 km apart. A test of alternate models of population history strongly favours a model of long-term drift-migration equilibrium over a recent isolation drift-only model. These results suggest that recent habitat fragmentation has had little effect on the genetic characteristics of these snakes, but rather that this species has historically existed in small isolated populations that may be resistant to the long-term negative effects of inbreeding.     

Habitat selection by grassland snakes at northern range limits: Implications for conservation

Animal populations at northern range limits may use habitat differently from those at range cores, requiring distinct conservation plans. Snakes are ectotherms that often have very specific requirements, but few studies have focused on the effect of northern latitudes on habitat selection by grassland snakes. We studied movement and habitat selection of 2 sympatric snake species at their northern range limits on the North American Great Plains: the eastern yellow-bellied racer (Coluber constrictor flaviventris, hereafter racer), a Threatened species in Canada, and the bullsnake (Pituophis catenifer sayi), which is listed as Data Deficient. Both of these species are potentially vulnerable to extinction in Canada because of habitat loss. Snakes from our study populations traveled up to 10-times farther from winter dens and occupied home ranges 3–104 times larger than populations further south. Both snake species moved from winter dens in the slopes of a major river valley to habitat in adjacent lowlands, including riparian zones (racers) and hilly areas with native grass species (bullsnakes). Multivariate modeling revealed that proximity to retreat sites was a significant predictor of snake site use for both species. Considering the need for winter dens and summering areas, our data suggest that snakes in northern latitudes should ideally have much larger protected areas compared to snakes near the core of their range. An alternative strategy is to conserve corridors linking wintering dens and summer habitats. Retreat sites such as burrows and shrubs are critical components of local habitat and should be included in conservation plans. © 2011 The Wildlife Society.     

Post-bite Elevation in Tongue-flick Rate by Neonatal Garter Snakes (Thamnophis radix)

A post-biting elevation in tongue-flicking rate was demonstrated experimentally in neonatal, ingestively naive garter snakes (Thamnophis radix). That the snakes also exhibited apparent searching movements suggests that strike-induced chemosensory searching occurs in nonvenomous snakes lacking previous experience with food or prey chemicals. Two litters of neonates differed in numbers of tongue-flicks emitted, but had similar relative magnitudes of response across experimental conditions. The existence of post-bite elevation in tongue-flick rate (and presumably strike-induced chemosensory searching) argues for a genetic basis for these chemosensory behaviors in a nonvenomous species of snake, extending the recent finding that strike-induced chemosensory searching is fully developed in ingestively naive neonatal rattlesnakes. Possible patterns of evolution of post-bite elevation in tongue-flick rate, and the strike-release-trail strategy of highly venomous snakes are discussed.     

A multiscale analysis of gene flow for the New England cottontail,an imperiled habitat specialist in a fragmented landscape

Landscape features of anthropogenic or natural origin can influence organisms' dispersal patterns and the connectivity of populations. Understanding these relationships is of broad interest in ecology and evolutionary biology and provides key insights for habitat conservation planning at the landscape scale. This knowledge is germane to restoration efforts for the New England cottontail (Sylvilagus transitionalis), an early successional habitat specialist of conservation concern. We evaluated local population structure and measures of genetic diversity of a geographically isolated population of cottontails in the northeastern United States. We also conducted a multiscale landscape genetic analysis, in which we assessed genetic discontinuities relative to the landscape and developed several resistance models to test hypotheses about landscape features that promote or inhibit cottontail dispersal within and across the local populations. Bayesian clustering identified four genetically distinct populations, with very little migration among them, and additional substructure within one of those populations. These populations had private alleles, low genetic diversity, critically low effective population sizes (3.2–36.7), and evidence of recent genetic bottlenecks. Major highways and a river were found to limit cottontail dispersal and to separate populations. The habitat along roadsides, railroad beds, and utility corridors, on the other hand, was found to facilitate cottontail movement among patches. The relative importance of dispersal barriers and facilitators on gene flow varied among populations in relation to landscape composition, demonstrating the complexity and context dependency of factors influencing gene flow and highlighting the importance of replication and scale in landscape genetic studies. Our findings provide information for the design of restoration landscapes for the New England cottontail and also highlight the dual influence of roads, as both barriers and facilitators of dispersal for an early successional habitat specialist in a fragmented landscape.     

Spatial genetic analysis of the grass snake,Natrix natrix (Squamata: Colubridae), in an intensively used agricultural landscape

Both the conversion of natural habitats to farmland and efforts at increasing the yield of existing crops contribute to a decline in biodiversity. As a consequence of land conversion, specialised species are restricted to remnants of original habitat patches, which are frequently isolated. This may lead to a genetic differentiation of the subpopulations. We used seven microsatellite markers to examine the genetic population structure of the grass snake, Natrix natrix (Linnaeus, 1758), sampled in remnants of pristine habitat embedded in an intensively used agricultural landscape in north‐western Switzerland. The study area, a former wetland, has been drained and gradually converted into an agricultural plain in the last century, reducing the pristine habitat to approximately 1% of the entire area. The grass snake feeds almost entirely on amphibians, and is therefore associated with wetlands. In Central Europe, the species shows severe decline, most probably as a result of wetland drainage and decrease of amphibian populations. We found no genetically distinct grass snake populations in the study area covering 90 km². This implies that there is an exchange of individuals between small remnants of original habitat. Thus, gene flow may prevent any genetic differentiation of subpopulations distributed over a relatively large area. Our results show that a specialized snake species can persist in an intensively used agricultural landscape, provided that suitable habitat patches are interconnected. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 51–58.     

Connectivity and gene flow among Eastern Tiger Salamander (Ambystoma tigrinum) populations in highly modified anthropogenic landscapes

Fragmented landscapes resulting from anthropogenic habitat modification can have significant impacts on dispersal, gene flow, and persistence of wildlife populations. Therefore, quantifying population connectivity across a mosaic of habitats in highly modified landscapes is critical for the development of conservation management plans for threatened populations. Endangered populations of the eastern tiger salamander (Ambystoma tigrinum) in New York and New Jersey are at the northern edge of the species’ range and remaining populations persist in highly developed landscapes in both states. We used landscape genetic approaches to examine regional genetic population structure and potential barriers to migration among remaining populations. Despite the post-glacial demographic processes that have shaped genetic diversity in tiger salamander populations at the northern extent of their range, we found that populations in each state belong to distinct genetic clusters, consistent with the large geographic distance that separates them. We detected overall low genetic diversity and high relatedness within populations, likely due to recent range expansion, isolation, and relatively small population sizes. Nonetheless, landscape connectivity analyses reveal habitat corridors among remaining breeding ponds. Furthermore, molecular estimates of population connectivity among ponds indicate that gene flow still occurs at regional scales. Further fragmentation of remaining habitat will potentially restrict dispersal among breeding ponds, cause the erosion of genetic diversity, and exacerbate already high levels of inbreeding. We recommend the continued management and maintenance of habitat corridors to ensure long-term viability of these endangered populations.