Thamnophis Species Research Articles

A new species of Thamnophis (Serpentes, Colubridae) from Jalisco, Mexico, with a discussion on the phylogeny, taxonomy, and distribution of snakes related to Thamnophis scalaris

Garter snakes in the genus Thamnophis from Mexico have a long and convoluted taxonomic history. From 2015 to 2022, we conducted a comprehensive sampling of Mexican Thamnophis species, aiming to link molecular phylogenies with the recognized species related to T. scalaris in the highlands of Mexico. Here, we present an analysis of mitochondrial DNA to resolve the status of two enigmatic highland Thamnophis populations. Our research resulted in the identification and morphological characterization of a previously undescribed Thamnophis species from the state of Jalisco in western Mexico. We also clarify the identity and relationships of several previously enigmatic populations of Thamnophis. This work presents new data for Thamnophis phylogenetics from the Mexican highlands and offers a framework for future conservation efforts.

The road not taken: Evolution of tetrodotoxin resistance in the Sierra garter snake (Thamnophis couchii) by a path less travelled.

The repeated evolution of tetrodotoxin (TTX) resistance provides a model for testing hypotheses about the mechanisms of convergent evolution. This poison is broadly employed as a potent antipredator defence, blocking voltage-gated sodium channels (Nav ) in muscles and nerves, paralysing and sometimes killing predators. Resistance in taxa bearing this neurotoxin and a few predators appears to come from convergent replacements in specific Nav residues that interact with TTX. This stereotyped genetic response suggests molecular and phenotypic evolution may be constrained and predictable. Here, we investigate the extent of mechanistic convergence in garter snakes (Thamnophis) that prey on TTX-bearing newts (Taricha) by examining the physiological and genetic basis of TTX resistance in the Sierra garter snake (Th.couchii). We characterize variation in this predatory adaptation across populations at several biological scales: whole-animal TTX resistance; skeletal muscle resistance; functional genetic variation in three Nav encoding loci; and levels of gene expression for one of these loci. We found Th.couchii possess extensive geographical variation in resistance at the whole-animal and skeletal muscle levels. As in other Thamnophis, resistance at both levels is highly correlated, suggesting convergence across the biological levels linking organism to organ. However, Th.couchii shows no functional variation in Nav loci among populations or difference in candidate gene expression. Local variation in TTX resistance in Th.couchii cannot be explained by the same relationship between genotype and phenotype seen in other taxa. Thus, historical contingencies may lead different species of Thamnophis down alternative routes to local adaptation.

HERPETOFAUNAL ASSEMBLAGE AND NATURAL HISTORY OF A WETLAND AND PRAIRIE COMPLEX OF THE NORTHERN GREAT PLAINS

Tallgrass prairies are some of the most imperiled ecosystems in North America, yet the herpetofauna found within these habitats are not well known. We studied the herpetofaunal assemblage of the Chichaqua Bottoms Greenbelt and Chichaqua Wildlife Management Area complex (CBG) in Iowa as well as the natural history of Thamnophis species. We found that the CBG housed substantial diversity with seven species of anurans, one species of salamander, three species of turtles, and nine species of snakes. Three Thamnophis species in the CBG differed in body size, diet, and both ambient temperature and time of day at capture. This research contributes to our knowledge of the diversity and natural history of herpetofauna in northern prairies.

Development of a quantitative polymerase chain reaction assay and environmental DNA sampling methods for Giant Gartersnake (Thamnophis gigas).

The Giant Gartersnake (Thamnophis gigas) is a low density visually evasive species with a low detection probability based on standard field survey methods (e.g., traps, visual census). Habitat loss has resulted in extirpations or serious declines for T. gigas populations throughout the southern two thirds of its historic range. Uncertainty regarding its current distribution and occupancy present management challenges for the species. Enhancing survey sensitivity through development of environmental DNA sampling (eDNA) methods would improve compliance monitoring under the Endangered Species Act, recovery planning for T. gigas, and evaluation of California’s Central Valley tule marsh habitat on which this species depends. To address these needs, we designed and validated diagnostic quantitative Polymerase Chain Reaction (qPCR) assays for identifying portions of the Cytochrome B (CytB) and the Nicotinamide adenine dinucleotide (NADH) dehydrogenase subunit 4 (ND4) genes of the T. gigas mitochondrial genome. The designed ND4 qPCR assay was not specific to T. gigas DNA and amplified DNA from a closely related and spatially co-occurring Thamnophis species (T.s. fitchi). The CytB T. gigas qPCR assay proved specific to a species level with a sensitivity that reliably detected T. gigas DNA at a concentration of 2.0x10-5 ng μL-1. To assess detection range, coordinated field sampling was conducted at aquatic sites with an observed and documented population of T. gigas. The T. gigas qPCR assay reliably detected DNA from samples taken 300m downstream from the known source. We then used environmental eDNA sampling and qPCR analysis to augment unsuccessful trap surveys in the southern range of T. gigas and detected DNA in 28 of the 52 locations sampled, confirming that T. gigas was still present at some sites where physical trapping failed to identify presence. QPCR-based DNA detection coupled with eDNA sampling methods provides an effective means to obtain critical population metrics from this otherwise cryptic, federally protected and hard to study organism, offering great promise for elucidating patterns of occupancy with greater efficiency and at far less cost than trapping methods, particularly where detection probabilities are low.

Present and future ecological niche modeling of garter snake species from the Trans-Mexican Volcanic Belt.

Land use and climate change are affecting the abundance and distribution of species. The Trans-Mexican Volcanic Belt (TMVB) is a very diverse region due to geological history, geographic position, and climate. It is also one of the most disturbed regions in Mexico. Reptiles are particularly sensitive to environmental changes due to their low dispersal capacity and thermal ecology. In this study, we define the important environmental variables (considering climate, topography, and land use) and potential distribution (present and future) of the five Thamnophis species present in TMVB. To do so, we used the maximum entropy modeling software (MAXENT). First, we modeled to select the most important variables to explain the distribution of each species, then we modeled again using only the most important variables and projected these models to the future considering a middle-moderate climate change scenario (rcp45), and land use and vegetation variables for the year 2050 (generated according to land use changes that occurred between years 2002 and 2011). Arid vegetation had an important negative effect on habitat suitability for all species, and minimum temperature of the coldest month was important for four of the five species. Thamnophis cyrtopsis was the species with the lowest tolerance to minimum temperatures. The maximum temperature of the warmest month was important for T. scalaris and T. cyrtopsis. Low percentages of agriculture were positive for T. eques and T. melanogaster but, at higher values, agriculture had a negative effect on habitat suitability for both species. Elevation was the most important variable to explain T. eques and T. melanogaster potential distribution while distance to Abies forests was the most important variable for T. scalaris and T. scaliger. All species had a high proportion of their potential distribution in the TMVB. However, according to our models, all Thamnophis species will experience reductions in their potential distribution in this region. T. scalaris will suffer the biggest reduction because this species is limited by high temperatures and will not be able to shift its distribution upward, as it is already present in the highest elevations of the TMVB.

Correlated evolution of sexually selected traits: interspecific variation in ejaculates, sperm morphology, copulatory mate guarding, and body size in two sympatric species of garter snakes

Male reproductive success is dependent on a correlated suite of traits related to a species’ ecology and mating system dynamics. Closely related species differing in their mating systems and ecology, such as the garter snakes (Thamnophis), are ideal for studying the correlated evolution of sexually selected traits. Here, we compare the degree of sexual size dimorphism (SSD), copulatory behavior, copulatory plug size, and traits associated with sperm competition between two sympatric and closely related Thamnophis species, T. sirtalis and T. radix with divergent mating aggregation size and density. Our findings indicate that T. sirtalis has greater female-biased SSD, shorter copulations, and larger, more strongly adhering copulatory plugs than T. radix. Our finding that T. sirtalis have longer sperm and higher numbers of sperm per ejaculate is further evidence of more intense sperm competition in this species than in T. radix. However, this reduced number of sperm in the ejaculate means that T. radix males are likely capable of more matings per season than T. sirtalis. This result may reflect differences in feeding during the breeding season (obligate aphagy in T. sirtalis) and the potential for sperm loss in T. radix during prolonged copulations that are prevented in T. sirtlais by their substantial copulatory plugs. Our findings demonstrate that ecological and mating system dynamics have the capacity to strongly influence correlated selection of pre- and postcopulatory traits. Our findings demonstrate that ecological and mating system dynamics have the capacity to strongly influence correlated selection of, and trade-offs between, pre- and postcopulatory traits. For most postcopulatory selected traits we measured (sperm size, ejaculate size, effectiveness of their copulatory plug, and gamete-somatic index (but not relative testes mass)), the species predicted to experience strong sperm competition (T. sirtalis) has higher trait values. However, T. radix, which has a precopulatory mating advantage (larger male body size and less pronounced female-biased sexual size dimorphism), has enough stored sperm for many more matings. The large amount of stored sperm in T. radix may be due to sperm loss during prolonged matings or different energy budgets between the two species: T. sirtalis, with an evolutionary history of sperm competition, does not eat during the breeding season, which limits the time available for mating.

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.

Evidence of Hybridization between Common Gartersnakes (Thamnophis sirtalis) and Butler's Gartersnakes (Thamnophis butleri) in Wisconsin, USA

Abstract Snakes within the genus Thamnophis (Gartersnakes and Ribbonsnakes) are often found in sympatry throughout their geographic distributions. Past work has indicated that some sympatric species within this genus may hybridize, but research of this nature is limited. We attempted to determine whether hybridization occurs between two Thamnophis species native to the upper midwestern United States: Common Gartersnake (Thamnophis sirtalis) and the Butler's Gartersnake (Thamnophis butleri). We sampled snakes (n = 411) across 26 locations in Wisconsin, including sites where both species coexist and sites where only Common Gartersnakes are found. We conducted genetic analyses on tissue collected from individuals field-identified as Common Gartersnakes or Butler's Gartersnakes. To verify the results of our field-collected data, we analyzed tissues from juvenile snakes (n = 4) suspected to be the offspring of a Common Gartersnake and a Butler's Gartersnake that were housed together in a captive situation. Of ...

Temporal dynamics of relative-mass variation of red-sided garter snakes (Thamnophis sirtalis parietalis) at a communal hibernaculum in Manitoba

An animal's relative body mass (i.e., mass adjusted for length or some other size dimension) is a potential indicator of its body condition, which in turn can influence demographic traits. In this study, I revisited data collected in 1969–1970 on garter snakes, Thamnophis sirtalis parietalis, at a communal hibernaculum in Manitoba, to test hypotheses generated by more recent literature. First, I compared fall-through-spring variation in relative mass to a similar study of another species of Thamnophis in a milder, Mediterranean climate and found a similar temporal pattern, suggesting common features across a wide latitudinal range. Female snakes had a higher relative mass than males and experienced lower decline in relative mass overwinter and through the spring. This suggests different hibernation strategies of the 2 sexes, possibly involving different temperatures or differences in metabolism, and also reflects the preoccupation of males upon spring emergence with searching for mates, at energetic cost while not feeding. Comparison of my data with a second study of the same species at another den in Manitoba indicated nearly identical patterns of loss of mass, based on recaptures of males throughout the spring, and also corroborated that study's finding that initially relatively heavy males remained at the den longer. Thus, males that have accumulated more capital the previous year presumably have more opportunities to mate. Although recapture intervals of most males were only a few days long, similar to the previous study, some males remained in the vicinity of the den for up to 5 weeks. These findings underscore the fundamental differences between males and females in the temporal distribution of their costs of reproduction.

Food Habits of the Plains Garter Snake (Thamnophis radix) at the Northern Limit of Its Range

The North American genus Thamnophis is a widely distributed and abundant group of snakes. Previous research has indicated that most garter snakes are generalist predators that largely consume anurans, with some degree of geographic and temporal plasticity in response to resource variation. We studied the dietary habits of the Plains Garter Snake, Thamnophis radix, based on stomach contents from 548 animals collected in the field from 1995-2006 at the northern limit of the species' range in central Alberta, Canada. Feeding frequency overall was low (22%) and was highest in spring and early summer. Diet was composed mainly of anurans (85%), especially Wood Frogs (Rana sylvatica) and Boreal Chorus Frogs (Pseudacris maculata), and occasionally invertebrates (10%) and small mammals (5%). Small snakes (<200 mm) began feeding shortly after birth and consumed mainly smaller frogs. Larger snakes ate a wider range of prey sizes and types, but frogs still constituted the majority of prey consumed. Despite sexual size dimorphism, males and females ate prey of the same size and type; however, gravid females contained food less frequently than both males and nongravid females. This study adds to the growing number of dietary studies on T. radix and provides additional evidence for the ecological plasticity of Thamnophis species. Further studies are needed to examine how important these snakes are as components of wetland food chains.

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

AbstractPrevious 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.

Placentation in garter snakes: scanning EM of the placental membranes of Thamnophis ordinoides and T. sirtalis.

Surface topography and cross-sections of the placental membranes were examined by scanning electron microscopy in two species of Thamnophis. The chorionic epithelium of the chorioallantoic placenta consists of broad, squamous cells that lack surface specializations. The apposed uterine epithelium contains ciliated cells and larger, nonciliated cells. Neither the epithelium of the chorion nor that of the uterus is eroded; thus, underlying capillaries are not exposed to the luminal surface. In both the omphaloplacenta and the omphalallantoic placenta, epithelium of the omphalopleure consists of brush-border cells bearing prominent microvilli, interspersed with cells bearing minuscule microvilli. These surface epithelial cells are joined at their apices and their lateral surfaces are extensively sculpted by intercellular channels, presenting the appearance of an epithelium specialized for absorption. Deep to the epithelium lie the yolk spheres of the isolated yolk mass, interspersed with endodermal cells. Surface topography of the uterine epithelia of the omphaloplacenta and omphalallantoic placenta is relatively unspecialized. The acellular shell membrane separates maternal and fetal tissues in each of the three placental types. Marked differences in surface features of the chorioallantois and omphalopleure probably reflect different roles of these membranes in gas exchange and transfer of water and nutrients.

Phylogenetic Relationships of North American Garter Snakes (Thamnophis) Based on Four Mitochondrial Genes: How Much DNA Sequence Is Enough?

The clade of garter snakes (Thamnophis) includes some of the most abundant and well-studied snakes in North America. However, phylogenetic relationships within this group have been little studied. We used DNA sequences of four mitochondrial genes (cytochrome b and NADH dehydrogenase subunits 1, 2, and 4) to estimate relationships among 29 of the 31 recognized species of Thamnophis plus the related species Adelophis foxi. Both maximum parsimony (MP) and maximum-likelihood (ML) analyses of all these genes combined produced well-resolved trees with moderate (70–89%) to strong (90–100%) bootstrap support for most clades. MP and ML trees were very similar, with no strongly supported conflict between the two analyses. These analyses identify a clade of 12 species largely restricted to México (the “Mexican clade”), and a clade containing 15 species that collectively range from Central America to southern Canada (the “widespread clade”). These two groups are identified as sister taxa in both MP and ML analyses. A clade consisting of the ribbon snakes (T. sauritus and T. proximus) and the common garter snake (T. sirtalis) is placed as the sister group to all other Thamnophis (i.e., the Mexican + widespread clades) in our analyses. High bootstrap proportions at several levels in the tree support the inclusion of both Thamnophis validus, which has traditionally been placed in the genus Nerodia, and the poorly known species Adelophis foxi within Thamnophis. We used randomly sampled characters (i.e., standard bootstrapping) and randomly sampled contiguous blocks of characters to examine the effect of number of characters on resolution of and support for relationships within Thamnophis using MP. In general, these analyses indicate that we have reached a point of strongly diminishing returns with respect to the effect of adding mtDNA sequence characters for the current set of taxa; our sample of 3809 mtDNA characters is apparently “enough.” The next steps to improve the phylogenetic estimate may be to add nuclear DNA sequences, morphology, or behavior, or to sequence additional mtDNA lineages within species.

The Inconsistent and Inefficient Constricting Behavior of Colorado Western Terrestrial Garter Snakes, Thamnophis elegans

The Inconsistent and Inefficient Constricting Behavior of Colorado Western Terrestrial Garter Snakes, Thamnophis elegans

Ecology of an Aquatic Snake (Thamnophis marcianus) in a Desert Environment: Implications of Early Timing of Birth and Geographic Variation in Reproduction

Abstract We studied the ecology of the checkered garter snake, Thamnophis marcianus, in a desert grassland in southeastern Arizona. The adult sex ratio was 0.67 M:F and varied significantly among seasons. As with other species of Thamnophis, adult females were significantly larger than males in SVL and body mass, and females also had longer jaws. Activity occurred both during the day and nighttime, but was confined to aquatic areas or their immediate vicinity. Mating occurred in late March and females gave birth to a single brood of an average of 15 offspring in late May and early June. The timing of birth in this population was among the earliest on record for any live-bearing snake in North America and was much earlier than for other checkered garter snake populations. In comparison with populations of T. marcianus from northern and southern Texas, females from Arizona had larger maternal body sizes and their offspring were larger as well; conversely, we found no significant differences in brood size am...

EVOLUTIONARY RESPONSE OF PREDATORS TO DANGEROUS PREY: PREADAPTATION AND THE EVOLUTION OF TETRODOTOXIN RESISTANCE IN GARTER SNAKES.

Coevolutionary interactions typically involve only a few specialized taxa. The factors that cause some taxa and not others to respond evolutionarily to selection by another species are poorly understood. Preadaptation may render some species predisposed for evolutionary response to new pressures, whereas a lack of genetic variation may limit the evolutionary potential of other taxa. We evaluate these factors in the predator-prey interaction between toxic newts (Taricha granulosa) and their resistant garter snake predators (Thamnophis sirtalis). Using a bioassay of resistance to tetrodotoxin (TTX), the primary toxin in the prey, we examined phenotypic evolution in the genus Thamnophis. Reconstruction of ancestral character states suggests that the entire genus Thamnophis, and possibly natricine snakes in general, has slightly elevated TTX resistance compared to other lineages of snakes. While this suggests that T. sirtalis is indeed predisposed to evolving TTX resistance, it also indicates that the potential exists in sympatric congeners not expressing elevated levels of TTX resistance. We also detected significant family level variation for TTX resistance in a species of Thamnophis that does not exhibit elaborated levels of the trait. This finding suggests that evolutionary response in other taxa is not limited by genetic variability. In this predator-prey system, species and population differences in resistance appear to be largely determined by variation in the selective environment rather than preadaptation or constraint.

Human envenomation from a wandering garter snake

Garter snake bites are generally innocuous to human beings. We report a case of human envenomation from the Wandering Garter snake (Thamnophis elegans vagrans). The patient, who was bitten on his right third fingertip, rapidly developed local edema, ecchymosis, and hemorrhagic vesicles. Systemic signs and symptoms did not develop. The clinical picture was similar to that in three previous patients with Thamnophis envenomation in that clinical signs followed a prolonged bite. Thamnophis species have Duvernoy's glands, which may be analogous to venom glands in Crotalidae (pit viper) species. The progressive local effects produced by secretions of these glands may be confused with early Crotalidae envenomation.

Comparative Field Study of Thermal Preferenda in Garter Snakes (Thamnophis)

Field body temperature records from seven species of Thamnophis were used to investigate intrageneric variation of body temperature selection under field conditions. There was no evidence for geographic or interspecific variation of thermal preferenda in Thamnophis. Major factors imposing con- straints or influencing body temperature were found to be season, weather, macrohabitat, time of day, reproductive status, and activity type. After controlling for these factors, field-selected body temperatures converged on an apparent intragenerically stable preferendum near 30 C, with means ranging from 28.04- 30.53 C for the study populations. Observations on thermoregulatory behavior suggest that behavioral adjustments compensate for thermal differences among habitats and across latitude. Review of the literature revealed that intrageneric variation of PBT in snakes has yet to be demonstrated unequivocally. The potential significance of, and possible reasons for, the conservatism of PBT in snakes are discussed in terms of stabilizing selection and plasticity of activity timing in the diel cycle. ABSTRACT. - Field body temperature records from seven species of Thamnophis were used to investigate intrageneric variation of body temperature selection under field conditions. There was no evidence for geographic or interspecific variation of thermal preferenda in Thamnophis. Major factors imposing con- straints or influencing body temperature were found to be season, weather, macrohabitat, time of day, reproductive status, and activity type. After controlling for these factors, field-selected body temperatures converged on an apparent intragenerically stable preferendum near 30 C, with means ranging from 28.04- 30.53 C for the study populations. Observations on thermoregulatory behavior suggest that behavioral adjustments compensate for thermal differences among habitats and across latitude. Review of the literature revealed that intrageneric variation of PBT in snakes has yet to be demonstrated unequivocally. The potential significance of, and possible reasons for, the conservatism of PBT in snakes are discussed in terms of stabilizing selection and plasticity of activity timing in the diel cycle.

Effects of sulfhydryl reagent, p-chloromercuribenzoate, on p-aminohippurate transport by isolated, perfused snake renal tubules.

Effects of mercaptide-forming sulfhydryl reagent, p-chloromercuribenzoate (PCMB), on transport of p-aminohippurate (PAH) by isolated, perfused snake (Thamnophis species) renal tubules were studied. PCMB (10(-7) mol/l) in bathing medium irreversibly inhibited net transepithelial transport of PAH (JPAH) without affecting net fluid absorption (Jv). PCMB (10(-8) mol/l) in perfusate irreversibly inhibited JPAH without affecting Jv and markedly reduced the apparent permeability of the luminal membrane to PAH. These data suggest that sulfhydryl groups may be involved in the PAH transport steps at both the peritubular and luminal membranes.

Tail Loss Patterns in Thamnophis (Reptilia: Colubridae) and the Probable Fate of Injured Individuals

The frequency of tail loss in three species of Thamnophis was evaluated. Significant sex and size dependencies of tail loss were found in T. sirtalis and T. sauritus, but not in T. butleri. Tail loss was greater in females than in males, and generally increased with size. The frequency of tail loss was reduced in the 2529 cm size class. Because smaller, injured individuals must be preferentially eliminated from the population for this reduction in tail loss frequency to occur, we hypothesized that injured juveniles do not survive their first year, possibly due to hibernation stress. Alternately, injured snakes may emigrate or have injury-related behavioral changes which result in reduced frequencies of recapture. However, no injured snake less than a year old was recaptured after its first year; the frequency of injury of recaptured snakes in larger size classes was not different from the frequency of injury in original captures, further suggesting that injury in first year snakes results in death before the second year.