Thamnophis Research Articles

Determinants and modeling of specific dynamic action for the Common Garter Snake (Thamnophis sirtalis)

Specific dynamic action (SDA), the cumulative energy expended on digestion and assimilation, can contribute significantly to individual daily energy expenditure (DEE). The Common Garter Snake (Thamnophis sirtalis (L., 1758)) is a widely distributed generalist predator that could experience considerable variation in SDA and hence the contribution of SDA to DEE. We examined the effects of meal size, meal type, and body temperature on the postprandial metabolic response and SDA of the Eastern Garter Snake ( Thamnophis sirtalis sirtalis (L., 1758)) and generated predictive models of SDA based on meal size, body mass, and body temperature, and separately based on meal energy. Postprandial peak in oxygen consumption, duration of significantly elevated oxygen consumption, and SDA increased with increasing meal size (5%–45% of body mass). Postprandial metabolic response digesting six different equal-size prey items varied significantly; vertebrate prey generated larger SDA responses than soft-bodied invertebrates. Increases in experimental temperature (15–35 °C) yielded a matched increase in postprandial peak in oxygen consumption and decrease in digestive duration. For a 1-month hypothetical feeding history for an adult T. sirtalis, the cumulative predicted SDA varied by 4.5% among the three models (minimal, intermediate, and maximal intake of prey) and averaged 8%, 22%, and 38% of DEE, respectively.

Temporally distinct effects of stress and corticosterone on diel melatonin rhythms of red-sided garter snakes ( Thamnophis sirtalis)

Circadian and circannual rhythms in physiology and behavior are temporally organized via hormonal signals that reflect changing environmental cues. Interactions between endocrine signals are in turn important for integrating multiple physiological and behavioral rhythms. In the present study, we examined interactions between melatonin, the hypothalamus–pituitary–adrenal (HPA) axis, and corticosterone in a well-studied population of red-sided garter snakes ( Thamnophis sirtalis parietalis). We demonstrate that 4 h of capture stress significantly increased photophasic melatonin and decreased scotophasic melatonin concentrations of male snakes. Treatment with exogenous corticosterone (15 and 60 μg) did not mimic the effects of stress on diel melatonin rhythms. To determine if capture stress decreases scotophasic melatonin by depleting the precursors necessary for melatonin synthesis, we used a paradigm in which snakes were treated with the melatonin precursor 5-hydroxytryptophan (0.6 and 1.2 mg) to elevate melatonin concentrations. Pretreatment of snakes with both capture stress and exogenous corticosterone blocked the effect of 5-hydroxytryptophan on scotophasic melatonin. Thus, although corticosterone itself does not influence melatonin rhythms of snakes, corticosterone can inhibit the synthesis of melatonin from 5-hydroxytryptophan. These experiments suggest that the initial versus later phases of an acute physiological stress response have temporally distinct effects on melatonin synthesis: activation of the sympathoadrenal system increases melatonin, while increased glucocorticoids can inhibit melatonin synthesis. Collectively, we demonstrate that a physiological coupling between melatonin, glucocorticoids, and the sympathoadrenal system is conserved in this ectothermic model and propose that such interactions may mediate stress-induced changes in physiology and behavior.

Social behavior and pheromonal communication in reptiles

The role of pheromones in orchestrating social behaviors in reptiles is reviewed. Although all reptile orders are examined, the vast majority of the literature has dealt only with squamates, primarily snakes and lizards. The literature is surprisingly large, but most studies have explored relatively few behaviors. The evolution of chemical signaling in reptiles is discussed along with behaviors governed by pheromones including conspecific trailing, male-male agonistic interactions, sex recognition and sex pheromones, and reptilian predator recognition. Nonreptilian prey recognition by chemical cues was not reviewed. The recent literature has focused on two model systems where extensive chemical ecology studies have been conducted: the reproductive ecology of garter snakes and the behavioral ecology of Iberian lacertid lizards. In these two systems, enough is known about the chemical constituents that mediate behaviors to explore the evolution of chemical signaling mechanisms that affect life history patterns. In addition, these models illuminate natural and sexual selection processes which have lead to complex chemical signals whose different components and concentrations provide essential information about individuals to conspecifics. Reptiles provide excellent candidates for further studies in this regard not only in squamates, but also in the orders where little experimental work has been conducted to date.

Discordant patterns of population structure for two co‐distributed snake species across a fragmented Ontario landscape

AbstractAim The goal of our study was to investigate the effects of a fragmented landscape on the genetic population structure of two sympatric snake species that differ in habitat preference. The eastern garter snake (Thamnophis sirtalis sirtalis) is a common, habitat generalist, whereas the endangered eastern foxsnake (Mintonius [Elaphe] gloydi) is rarer, geographically restricted, and a marsh‐specialist. We were most interested in comparing the genetic population structure of both species and identifying any natural and human‐created features of the landscape that overlap with genetic disjunctions.Location Southwestern Ontario, Canada, surveying over half of the remaining range of the eastern foxsnake.Methods We utilized DNA microsatellite markers to examine genetic population structure of both species. The number of genetically distinct clusters for each species was determined using both Bayesian spatial assignment and spatial principal component analyses (sPCA). Genetic clusters were overlaid onto a habitat map to deduce possible physiognomic barriers to gene flow.Results Spatial assignment revealed three genetic clusters for garter snakes and five for foxsnakes. Each individual garter snake had a near equal probability of membership to two or more clusters with no cluster mapping onto a discrete geographic region, indicating that garter snakes comprise a single genetic population. The identified foxsnake clusters correspond to geographically circumscribed locations on the landscape, roughly coincident with isolated patches of suitable habitat. sPCAs revealed significant global allelic structure for foxsnakes, but not for garter snakes. No significant local structure was found for either species.Main Conclusions Our results imply that foxsnakes and garter snakes are differentially impacted by the same landscape or have dramatically different effective population sizes. Unsuitable intervening habitat such as agricultural tracts and roads between existing populations of foxsnakes appears to act as barriers to gene flow, while garter snake movement appears unrestricted by these features. Our findings have important implications for the management of eastern foxsnakes.

Genetic architecture of a feeding adaptation: garter snake (Thamnophis) resistance to tetrodotoxin bearing prey.

Detailing the genetic basis of adaptive variation in natural populations is a first step towards understanding the process of adaptive evolution, yet few ecologically relevant traits have been characterized at the genetic level in wild populations. Traits that mediate coevolutionary interactions between species are ideal for studying adaptation because of the intensity of selection and the well-characterized ecological context. We have previously described the ecological context, evolutionary history and partial genetic basis of tetrodotoxin (TTX) resistance in garter snakes (Thamnophis). Derived mutations in a voltage-gated sodium channel gene (Na(v)1.4) in three garter snake species are associated with resistance to TTX, the lethal neurotoxin found in their newt prey (Taricha). Here we evaluate the contribution of Na(v)1.4 alleles to TTX resistance in two of those species from central coastal California. We measured the phenotypes (TTX resistance) and genotypes (Na(v)1.4 and microsatellites) in a local sample of Thamnophis atratus and Thamnophis sirtalis. Allelic variation in Na(v)1.4 explains 23 per cent of the variation in TTX resistance in T. atratus while variation in a haphazard sample of the genome (neutral microsatellite markers) shows no association with the phenotype. Similarly, allelic variation in Na(v)1.4 correlates almost perfectly with TTX resistance in T. sirtalis, but neutral variation does not. These strong correlations suggest that Na(v)1.4 is a major effect locus. The simple genetic architecture of TTX resistance in garter snakes may significantly impact the dynamics of phenotypic coevolution. Fixation of a few alleles of major effect in some garter snake populations may have led to the evolution of extreme phenotypes and an 'escape' from the arms race with newts.

Molecular Evidence for Parthenogenesis in the Sierra Garter Snake, Thamnophis couchii (Colubridae)

Abstract We used microsatellite analysis to investigate possible reproduction by parthenogenesis in the bisexual Sierra garter snake, Thamnophis couchii. The genotypes of four microsatellite loci were determined for each of four individuals, including three T. couchii, two of which were a female and her offspring, and T. ordinoides. The female T. couchii and her offspring were homozygous and identical for all four microsatellite loci; however, Ts3 and Ts4 are the only loci that supported reproduction by parthenogenesis as Ts1 and Ts2 were uninformative. These data along with absence of a unique paternal allele and known absence of an opportunity to mate prior to and during captivity is consistent with reproduction by parthenogenesis.

Quantitative Genetics of Pigmentation Development in 2 Populations of the Common Garter Snake, Thamnophis sirtalis

The evolutionary importance of ontogenetic change has been noted since Darwin. However, most analyses of phenotypic evolution focus on single landmark ages. Here, we present an inheritance study that quantifies genetic variation in pigmentation across early-age (i.e., birth to 180 days) development in 2 populations of the common garter snake, Thamnophis sirtalis. The populations are phenotypically distinct and geographically isolated (Manitoba, CA and Northern California, USA). There were highly significant differences between populations for the developmental trajectory of mean pigmentation, with the Manitoba population exhibiting a mean pigmentation level that increased across ontogeny, whereas the California population exhibited mean pigmentation that was invariant across ontogeny. Subsequent quantitative genetic analyses revealed heritable variation at all ages in Manitoba but low levels of phenotypic and genetic variation in California at all ages. A quantitative genetic decomposition of the longitudinal genetic variance-covariance matrix for the age-specific pigmentation phenotypes in the Manitoba population revealed 2 primary orthogonal axes that explained most ( approximately 100%) of the pigmentation variation across ontogeny. The primary axis, explaining 93% of the genetic variation, is an axis of genetic variation whose principal value loadings change from positive to negative across development, suggesting that the most rapid evolutionary response to selection on pigmentation variation will occur in the direction characterized by a tradeoff in early-age versus late-age pigmentation phenotypes. Pigmentation is known to be ecologically important and subject to rapid evolution under selection. Our study shows that significant differences exist between these 2 populations for their capacity to respond to selection on pigmentation which is not only influenced by the population of origin but also by the developmental process. We suggest that developmental timing may be a potential explanatory mechanism for the difference between the populations.

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.

Seasonal aromatase activity in the brain of the male red-sided garter snake

We investigated regional and seasonal variations in neural aromatase activity (AA), the enzyme that converts androgens into estrogens, to examine a possible indirect role of testosterone (T) in mediating spring reproductive behavior of red-sided garter snakes, a species exhibiting a dissociated reproductive pattern. Neural AA in male snakes varied significantly among brain regions. Additionally, there were significant interactions between brain region and season. In the spring, actively courting males had greater AA in the olfactory region (O) compared to the septum/anterior-hypothalamus preoptic area (S/AHPOA), nucleus sphericus (NS) and midbrain (Mb). Fall animals collected as they returned to the den prior to winter dormancy had significantly greater AA in the S/AHPOA compared to all other regions. These findings were consistent using either regional (gross) dissection or punch microdissection, which allowed us to separate the S and AHPOA. There were no significant differences in AA production between the S and AHPOA. This study provides the first documentation of seasonal and regional variations in AA in a snake brain and suggests that aromatization of androgens may play a role in regulating reproduction in red-sided garter snakes. During spring mating, elevated AA in the O may activate pathways essential for detection of courtship pheromones, while increased AA in the S and AHPOA of fall animals suggests that circulating androgens play an indirect role in programming critical neural pathways involved in reproduction. Thus, as in many other vertebrates, estrogenic metabolites of testosterone may be a critical hormonal component regulating reproductive behavior in this dissociated breeder.

Erythrism in the Maritime Garter Snake, <em>Thamnophis sirtalis pallidulus</em>, in Nova Scotia

The Maritime Garter Snake, Thamnophis sirtalis pallidulus, is highly variable in pattern and colour. Although this subspecies is largely defined on the basis of colour, four colour morphs have previously been described for the subspecies, including a melanistic form. Based on specimens from Nova Scotia, Canada, a fifth, uncommon erythristic variant is added to the complex colour variation known for the Maritime Garter Snake. Erratum for figure included.

Evolution of Senescence in Nature: Physiological Evolution in Populations of Garter Snake with Divergent Life Histories

Evolutionary theories of aging are linked to life-history theory in that age-specific schedules of reproduction and survival determine the trajectory of age-specific mutation/selection balances across the life span and thus the rate of senescence. This is predicted to manifest at the organismal level in the evolution of energy allocation strategies of investing in somatic maintenance and robust stress responses in less hazardous environments in exchange for energy spent on growth and reproduction. Here we report experiments from long-studied populations of western terrestrial garter snakes (Thamnophis elegans) that reside in low and high extrinsic mortality environments, with evolved long and short life spans, respectively. Laboratory common-environment colonies of these two ecotypes were tested for a suite of physiological traits after control and stressed gestations. In offspring derived from control and corticosterone-treated dams, we measured resting metabolism; mitochondrial oxygen consumption, ATP and free radical production rates; and erythrocyte DNA damage and repair ability. We evaluated whether these aging biomarkers mirrored the evolution of life span and whether they were sensitive to stress. Neonates from the long-lived ecotype (1) were smaller, (2) consumed equal amounts of oxygen when corrected for body mass, (3) had DNA that damaged more readily but repaired more efficiently, and (4) had more efficient mitochondria and more efficient cellular antioxidant defenses than short-lived snakes. Many ecotype differences were enhanced in offspring derived from stress-treated dams, which supports the conclusion that nongenetic maternal effects may further impact the cellular stress defenses of offspring. Our findings reveal that physiological evolution underpins reptilian life histories and sheds light on the connectedness between stress response and aging pathways in wild-dwelling organisms.

The Biophysical Costs Associated With Tetrodotoxin Resistance in the Garter Snake, Thamnophis Sirtalis

Tetrodotoxin (TTX) is a potent toxin that specifically binds to voltage gated sodium channels (NaV). TTX binding physically blocks the flow of sodium ions through NaV, thereby preventing action potential generation and propagation. Populations of the garter snake, Thamnophis sirtalis, have evolved TTX resistance by substituting amino acid residues in the highly conversed domain IV P-loop of NaV1.4, allowing them to feed on tetrodotoxic newts. Different populations of the garter snake have different degrees of TTX-resistance closely related to the number of amino acid substitutions. Here, we tested the voltage dependence, kinetics, and ion selectivity of NaV1.4 containing sequences from different garter snake populations. Using Xenopus oocytes under cut-open voltage clamp, we observed significant changes in voltage dependent gating properties of the TTX resistant NaV. The most TTX-resistant channel had hyperpolarized activation midpoint (−6 mV) compared to TTX-sensitive channels. Fast inactivation of the TTX-resistant NaV had significant depolarizing shifts of 2.2 mV in mildly TTX-resistant channels, and 4.5 mV in strongly TTX-resistant channels. Depolarizing shifts in slow inactivation were also observed in TTX-resistant channels with 20 mV and 16 mV shifts in mildly resistant and strongly resistant channels, respectively. In addition, ion selectivity and permeability of TTX-resistant channels were significantly different from those of the TTX-sensitive channel. These results suggest TTX resistance comes at a cost to channel performance caused by changes in the gating properties and ion selectivity of TTX-resistant sodium channels.Supported by a NSERC Discovery Grant to PCR.

Identical Skin Toxins by Convergent Molecular Adaptation in Frogs

The Tree of Life is rife with adaptive convergences at all scales and biological levels of complexity. However, natural selection is not likely to result in the independent evolution of identical gene products. Here we report such a striking example of evolutionary convergence in the toxic skin secretions of two distantly related frog lineages. Caeruleins are important decapeptides in pharmacological and clinical research [1] and are commonly believed to represent a single evolutionary class of peptides [2-4]. Instead, our phylogenetic analyses combining transcriptome and genome data reveal that independently evolved precursor genes encode identical caeruleins in Xenopus and Litoria frogs. The former arose by duplication from the cholecystokinin (cck) gene, whereas the latter was derived from the gastrin gene. These hormone genes that are involved in many physiological processes diverged early in vertebrate evolution, after a segmental duplication during the Cambrian period. Besides implicating convergent mutations of the peptide-encoding sequence, recurrent caerulein origins entail parallel shifts of expression from the gut-brain axis to skin secretory glands. These results highlight extreme structural convergence in anciently diverged genes as an evolutionary mechanism through which recurrent adaptation is attained across large phylogenetic distances.

Ecology of a Population of the Narrow-Headed Garter Snake (Thamnophis rufipunctatus) in New Mexico: Catastrophic Decline of a River Specialist

Abstract We studied natural history and ecology of Thamnophis rufipunctatus at San Francisco Hot Springs, Catron County, New Mexico. Gee minnow traps were more effective at sampling adults than opportunistic captures. Females were larger than males in snout–vent length and mass, but males had longer tails. Although females were larger, rates of growth for juvenile males and females were similar. In 1996, the population was ca. 7.2 adult snakes/ha; however, we did not detect snakes in subsequent visits. Thamnophis rufipunctatus was most likely to be captured at sites with steep riverbed slope and large rocks of uniform size. Diet was exclusively fish, of which a large proportion was the introduced Gambusia affinis. This population of T. rufipunctatus was one of the most robust in the United States and it has completely disappeared in <10 years.

Carrion decomposition and nutrient cycling in a semiarid shrub–steppe ecosystem

Vertebrate carrion decomposition and nutrient cycling have both direct and indirect effects on the soil properties, fauna, and flora associated with an animal's carcass. While few comprehensive quantitative studies have been undertaken, those that have show considerable variability in decomposition processes and rates, their regulating variables, and the resultant ecosystem effects. In this two‐part study, decomposition rates of vertebrate species were measured in a semiarid, shrub–steppe environment (Wyoming, USA). First, decomposition loss rates of mass, energy, and nutrients were measured for rat carcasses (Rattus norvegicus) in four seasons and two microsites (surface and underground burrows). Decomposition rates varied significantly between microsites (burrow &gt; surface in spring and summer) and among seasons (spring &gt; summer &gt; autumn ≈ winter), with mass loss amounts linearly correlated with ambient air temperatures. Energy and nutrient losses were related to phased carcass organ/tissue losses, with energy, K, Na, N, and S being lost more quickly than skeletal components (P, Mg, Ca). Overall, the nutrient loss sequence was K = Na &gt; N = S &gt; P = Mg &gt; Ca. Carcass quality (N concentration) declined through time as a function of decay stage. Second, decomposition rates of 10 vertebrate species (mule deer [Odocoileus hemionus], dog [Canis familiaris], white‐tailed jackrabbit [Lepus townsendii], Uinta ground squirrel [Spermophilus armatus], least chipmunk [Tamias minimus], deer mouse [Peromyscus maniculatus], Magpie [Pica hudsonia], Sage Sparrow [Amphispiza belli], terrestrial garter snake [Thamnophis elegans], and northern leopard frog [Lithobates pipiens]) were measured with vertebrate scavengers present or absent. Mass loss rates varied among species and were generally faster in the presence of scavengers. Carcass body mass, N content, or labile/recalcitrant fractions did not correlate with decomposition rate, though surface area to volume ratios of mammal carcasses were positively correlated with wet‐mass decomposition rate. Nutrient measures of sub‐carcass soils showed soil N, P, and Na increased during decomposition. Increased soil nutrient amounts represented up to 15.6% of the available carcass N, 28.8% of carcass P, and 28.7% of carcass Na. At a landscape scale in the shrub–steppe ecosystem, carrion decomposition constituted &lt;1% of the nutrient‐cycling budget but contributed significantly to localized soil nutrient dynamics.

A test of life‐history theories of immune defence in two ecotypes of the garter snake, Thamnophis elegans

1. Life-history theorists have long observed that fast growth and high reproduction tend to be associated with short life span, suggesting that greater investment in such traits may trade off with self-maintenance. The immune system plays an integral role in self-maintenance and has been proposed as a mediator of life-history trade-offs. 2. Ecoimmunologists have predicted that fast-living organisms should rely more heavily on constitutive innate immunity than slow-living organisms, as constitutive innate defences are thought to be relatively inexpensive to develop and can provide a rapid, general response to pathogens. 3. We present the first study to examine this hypothesis in an ectothermic vertebrate, by testing for differences in three aspects of constitutive innate immunity in replicate populations of two life-history ecotypes of the garter snake Thamnophis elegans, one fast-living and one slow-living. 4. As predicted, free-ranging snakes from the fast-living ecotype had higher levels of all three measures of constitutive innate immunity than the slow-living ecotype. These differences in immunity were not explained by parasite loads measured. Furthermore, both ecotypes exhibited a positive relationship between innate immunity and body size/age, which we discuss in the context of ectotherm physiology and ecotype differences in developmental rates.

Low Temperature Dormancy Affects the Quantity and Quality of the Female Sexual Attractiveness Pheromone in Red-sided Garter Snakes

Low temperature dormancy is a necessary requirement of the annual cycle of most nonmigratory, temperate vertebrates. The red-sided garter snake, Thamnophis sirtalis parietalis, overwinters in communal dens during its prolonged winter dormancy (8 mo), and upon emergence, reproductive behavior of both sexes is maximal. Previous work on this species showed that male courtship behavior is maximally induced after simulated low temperature dormancy. The purpose of this study was to determine whether low temperature dormancy affects the pheromone profiles of individual female red-sided garter snakes. We collected females in the fall at den sites in Manitoba, Canada, and extracted pheromones from individuals at three different time points: fall (field), winter (lab), and spring (lab). Total skin lipid and pheromone fraction masses increased from fall to spring, and pheromone profiles were distinctly different in the fall and spring. Pheromone profiles became dominated by the long-chain, unsaturated methyl ketone components of the blend by the time snakes emerged in the spring. Further, the amounts of both saturated and unsaturated components increased from fall to spring, suggesting significant sex pheromone synthesis was induced by low temperature dormancy.

Endocrine mechanisms mediating temperature-induced reproductive behavior in red-sided garter snakes (Thamnophis sirtalis parietalis)

We investigated the mechanisms by which temperature induces seasonal reproductive behavior in red-sided garter snakes (Thamnophis sirtalis parietalis). Specifically, we addressed whether elevated temperatures during winter dormancy influence (1) diel melatonin and corticosterone rhythms; (2) sex steroid hormone and corticosterone profiles; and (3) the expression of reproductive behavior following emergence. Elevated hibernation temperatures (i.e. 10 degrees C versus 5 degrees C) significantly increased overall melatonin and decreased corticosterone concentrations of snakes. The temperature-induced differences in melatonin rhythms between the 5 degrees C and 10 degrees C treatment groups persisted even after both groups were again acclimated to 10 degrees C, indicating that cold temperature exposure has a lasting influence on melatonin rhythms. Elevated hibernation temperatures also significantly altered androgen and corticosterone profiles of snakes, providing a potential mechanism to explain reported annual variation in steroid hormones. Although previous studies indicate that male red-sided garter snakes exhibit a dissociated reproductive strategy, we demonstrate the presence of intersexual variation in sex steroid hormone profiles, as estradiol concentrations of female snakes increased significantly prior to spring mating activity. Importantly, the percentage change in body mass did not differ significantly between snakes in the hibernation treatments, indicating that the observed changes in hormone profiles are indeed temperature induced and not simply an indirect result of significant changes in the energy balance of snakes. Finally, in males maintained at 10 degrees C during winter dormancy the onset of courtship behavior following emergence was delayed. Our results suggest that environmental temperatures induce reproductive behavior, in part, via changes in diel melatonin and/or corticosterone rhythms in this seasonally breeding reptile.

The evolutionary origins of beneficial alleles during the repeated adaptation of garter snakes to deadly prey

Where do the genetic variants underlying adaptive change come from? Are currently adaptive alleles recruited by selection from standing genetic variation within populations, moved through introgression from other populations, or do they arise as novel mutations? Here, we examine the molecular basis of repeated adaptation to the toxin of deadly prey in 3 species of garter snakes (Thamnophis) to determine whether adaptation has evolved through novel mutations, sieving of existing variation, or transmission of beneficial alleles across species. Functional amino acid substitutions in the skeletal muscle sodium channel (Na(v)1.4) are largely responsible for the physiological resistance of garter snakes to tetrodotoxin found in their newt (Taricha) prey. Phylogenetic analyses reject the hypotheses that the unique resistance alleles observed in multiple Thamnophis species were present before the split of these lineages, or that alleles were shared among species through occasional hybridization events. Our results demonstrate that adaptive evolution has occurred independently multiple times in garter snakes via the de novo acquisition of beneficial mutations.

Dental Morphologies in Gartersnakes (Thamnophis) and Their Connection to Dietary Preferences

We examined morphological variation in tooth structure in four populations of garter snakes (genus Thamnophis) with diverse feeding habits and tested the hypothesis that morphological homoplasy evolved in the malacophagous predators Thamnophis ordinoides and Thamnophis elegans terrestris. Although long, slender teeth are typical in Neotropical colubrid snake species that prey on slugs and snails, this morphological feature did not occur in T. ordinoides and T. e. terrestris relative to closely related garter snakes (the diet generalist Thamnophis elegans elegans and piscivore Thamnophis couchii). However, we did find pronounced posterior ridges located on the posterior maxillary teeth in the two slug predators but not in the generalist feeders. The evolutionary origin and functional advantage of these ridges has yet to be identified. The fish specialist T. couchii has many morphological features characteristic of adaptations for piscivory, such as long, sharper teeth and elongated mandible bones.