Gene flow and melanism in garter snakes revisited: a comparison of molecular markers and island vs. coalescent models

Within populations, the stochastic effect of genetic drift and deterministic effect of natural selection are potentially weakened or altered by gene flow among populations. The influence of gene flow on Lake Erie populations of the common garter snake has been of particular interest because of a discontinuous colour pattern polymorphism (striped vs. melanistic) that is a target of natural selection. We reassessed the relative contributions of gene flow and genetic drift using genetic data and population size estimates. We compared all combinations of two marker systems and two analytical approaches to the estimation of gene flow rates: allozymes (data previously published), microsatellite DNA (new data), the island model ( F _ST-based approach), and a coalescence-based approach. For the coalescence approach, mutation rates and sampling effects were also investigated. While the two markers produced similar results, gene flow based on F _ST was considerably higher (Nm > 4) than that from the coalescence-based method (Nm < 1). Estimates of gene flow are likely to be inflated by lack of migration-drift equilibrium and changing population size. Potentially low rates of gene flow (Nm < 1), small population size at some sites, and positive correlations of number of microsatellite DNA alleles and island size and between M , mean ratio of number of alleles to range in allele size, and island size suggest that in addition to selection, random genetic drift may influence colour pattern frequencies. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79, 389–399.     

The evolutionary response of predators to dangerous prey: hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts

The "geographic mosaic" approach to understanding coevolution is predicated on the existence of variable selection across the landscape of an interaction between species. A range of ecological factors, from differences in resource availability to differences in community composition, can generate such a mosaic of selection among populations, and thereby differences in the strength of coevolution. The result is a mixture of hotspots, where reciprocal selection is strong, and coldspots, where reciprocal selection is weak or absent, throughout the ranges of species. Population subdivision further provides the opportunity for nonadaptive forces, including gene flow, drift, and metapopulation dynamics, to influence the coevolutionary interaction between species. Some predicted results of this geographic mosaic of coevolution include maladapted or mismatched phenotypes, maintenance of high levels of polymorphism, and prevention of stable equilibrium trait combinations. To evaluate the potential for the geographic mosaic to influence predator-prey coevolution, we investigated the geographic pattern of genetically determined TTX resistance in the garter snake Thamnophis sirtalis over much of the range of its ecological interaction with toxic newts of genus Taricha. We assayed TTX resistance in over 2900 garter snakes representing 333 families from 40 populations throughout western North America. Our results provide dramatic evidence that geographic structure is an important component in coevolutionary interactions between predators and prey. Resistance levels vary substantially (over three orders of magnitude) among populations and over short distances. The spatial array of variation is consistent with two areas of intense evolutionary response by predators ("hotspots") surrounded by clines of decreasing resistance. Some general predictions of the geographic mosaic process are supported, including clinal variation in phenotypes, polymorphism in some populations, and divergent outcomes of the interaction between predator and prey. Conversely, our data provide little support for one of the major predictions, mismatched values of interacting traits. Two lines of evidence suggest selection is paramount in determining population variation in resistance. First, phylogenetic information indicates that two hotspots of TTX resistance have evolved independently. Second, in the one region that TTX levels in prey have been quantified, resistance and toxicity levels match almost perfectly over a wide phenotypic and geographic range. However, these results do not preclude the role the nonadaptive forces in generating the overall geographic mosaic of TTX resistance. Much work remains to fill in the geographic pattern of variation among prey populations and, just as importantly, to explore the variation in the ecology of the interaction that occurs within populations.     

Behavioral shifts associated with reproduction in garter snakes

Reproduction may involve profound modifications to behaviorssuch as feeding, antipredator tactics, and thermoregulation.Such shifts have generally been interpreted as direct consequencesof reproduction but may instead be secondary effects of reproduction-associatedchanges in other traits such as habitat use. We quantified behaviorsof red-sided garter snakes (Thamnophis sirtalis parietalis)courting and mating at a communal den, and also of postreproductivesnakes dispersing from the same den. Snakes at the den activelycourted, did not feed, tolerated close approach by humans, anddid not retaliate (bite) when seized by us. Dispersing snakesdid not court, fed, fled from our approach, and bit when seized.Snakes of both groups were then transferred to outdoor arenasand retested. Courtship vigor by males, and attractiveness offemales, had declined but not disappeared for the dispersingsnakes. Snakes of both groups ate readily, showing that reproduction-associatedanorexia was a facultative response to lack of prey in the den.Body temperature regimes were also similar in the two groupsof snakes. Overall, many of the characteristic behavioral changesassociated with reproduction were responses to features of theden environment (e.g., presence of sexual partners, lack offood) rather than to reproduction per se. The shift in antipredatorresponses, however, may reflect a neural or endocrine "switch,"suggesting that the link between reproduction and other behaviorsinvolves a diversity of proximate mechanisms.     

Molecular phylogeography of common garter snakes (Thamnophis sirtalis) in western North America: implications for regional historical forces

Complete ND2 and partial ND4 and cytochrome b mitochondrial DNA (mtDNA) sequences were analysed to evaluate the phylogeographic patterns of common garter snakes (Thamnophis sirtalis) in western North America. This species is widely distributed throughout North America, and exhibits extensive phenotypic variation in the westernmost part of its range. The overall phylogeographic pattern based on mtDNA sequences is concordant with results from studies of other species in this region, implicating historical vicariant processes during the Pleistocene and indicating bottleneck effects of recent dispersal into postglacial habitat. Indeed, the topology is statistically consistent with the hypothesis of both southern (Great Basin and California) and northern (Haida Gwaii) refugia. Specifically, we identified genetic breaks among three major clades: Northwest Coastal populations, Intermountain populations, and all California populations. The California clade contained the only other well-supported branching patterns detected; relationships among populations within the two northern clades were indistinguishable. These molecular splits contrast sharply with all prior geographical analyses of phenotypic variation in T. sirtalis in this region. Our results suggest that the extensive phenotypic variation in western T. sirtalis has been shaped more by local evolutionary forces than by shared common ancestry. Consequently, we consider all morphologically based subspecies designations of T. sirtalis in this region invalid because they do not reflect reciprocal monophyly of the mtDNA sequences.     

Experimental evidence for the adaptive evolution of growth rate in the garter snake Thamnophis elegans

The western terrestrial garter snake (Thamnophis elegans) varies significantly in individual growth rates and life-history traits (maturation, reproduction, and survival) among adjacent populations in nature. This study focuses on assessing the genetic and environmental components of the substantial among-population variation in growth rates. Litters of neonates from nine populations inhabiting either mountain meadow or lakeshore habitat were reared for one year in a common-garden experiment with two temperature treatments. Diet, frequency of feeding, light exposure, and daytime temperatures were identical for all individuals. The two different nighttime temperatures (20 degrees C and 25 degrees C) were chosen to mirror field differences in nighttime thermoregulatory constraints for mountain-meadow and lakeshore snakes, respectively. Temperature and source habitat interacted to affect first-year growth rate. Neonates from meadow dams grew fastest in the cooler treatment, whereas those from lakeshore dams grew fastest in the warmer treatment. The observation that naive neonates, which were gestated and raised under identical conditions, grew fastest in environments characteristic of their natal population is evidence both that there are genetic differences among populations for growth and that these differences reflect adaptation to local habitats at a very small geographic scale. In addition, significant directional selection for large birthweight was measured for neonates from all populations. These results are considered in the context of population colonization history, migration and selection, and competing models for growth rate variation.     

Comparison of cranial form and function in association with diet in natricine snakes

The skull of squamates has many functions, with food acquisition and ingestion being paramount. Snakes vary interspecifically in the frequency, size, and types of prey that are consumed. Natural selection should favor phenotypes that minimize the costs of energy acquisition; therefore, trophic morphology should reflect a snake's primary prey type to enhance some aspect of feeding performance. I measured 19 cranial variables for six natricine species that vary in the frequency with which they consume frogs and fish. Both conventional and phylogenetically corrected analyses indicated that fish‐eating snakes have relatively longer upper and lower jaw elements than frog‐eating snakes, which tended to have broader skull components. I also compared the ratio of the in‐lever to the out‐lever lengths of the jaw‐closing mechanism [jaw mechanical advantage (MA)] among species. Fish‐eating snakes had significantly lower MAs in the jaws than did the frog‐eating snakes. This result suggests that piscivores have faster closing jaws and that the jaws of frog‐eating snakes have higher closing forces. Cranial morphology and the functional demands of prey capture and ingestion appear to be associated with primary prey type in natricine snakes. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Behavioural correlates with hemipenis morphology in New World natricine snakes

Copulatory organs (hemipenes) of male snakes vary markedly among species in shape and ornamentation. We suggest that sexual conflict over copulation duration may have shaped the evolution of hemipenis morphology, favouring more elaborate organs in species in which a long duration of copulation is especially beneficial to males, despite the associated costs to females. To test this proposition, we compare mating behaviour between two species of gartersnakes differing in hemipenis morphology. In addition, we review data on copulation duration and hemipenis morphology and relate hemipenis morphology to phylogeny among of New World natricines. As predicted, copulation duration was significantly shorter in the common gartersnake ( Thamnophis sirtalis ), a species with simple subcylindrical hemipenes, than in the plains gartersnake ( Thamnophis radix ), a species with more complex, bilobed organs. Furthermore, female T. radix frequently exhibited vigorous body rolls during copulation, a behaviour associated with copulation termination, whereas female T. sirtalis never exhibited this behaviour. Copulations were of shorter duration when female T. radix (but not T. sirtalis ) more greatly exceeded males in body size, suggesting that females can more easily disengage from small males. Our review of New World natricines provides only weak evidence for an association between copulation duration and hemipenis morphology. Our mapping of hemipenis morphology onto the New World natricine phylogeny suggests that hemipenis morphology is evolutionarily plastic; both simple and bilobed hemipenes occur in all three major natricine clades, as well as in two of three gartersnake subclades and several sister-species pairs.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 110–120.     

Geographic variation in the garter snakes (Thamnophis sirtalis) of the north-central United States, a multivariate study

A study of geographic variation in three subspecies of garter snake (Thamnophis sirtalis sirtalis, T. s. parietalis, T. s. semifasciata) in the north-central United States indicates patterns of irregular non-clinal microgeographic variation for 40 characters of coloration, scalation, and internal anatomy. Multivariate analyses show that geographically close populations are not always phenetically close and that overall differentiation of the phenotype is greater in males than in females. Univariate and multivariate studies indicate that T. s. semifasciata Cope 1892, restricted to the Chicago area, is not uniform within its small range and that it has no constant distinguishing features: it is shown to be taxonomically invalid.     

Metabolic costs of growth in free-living Garter Snakes and the energy budgets of ectotherms

1. The metabolic or respiratory cost of growth ( R _G) is the increase in metabolic rate of a growing animal, and it represents chemical potential energy expended in support of net biosynthesis but not deposited as new tissue.
2. Two statistical methods (multiple non-linear regression and analysis of regression residuals) were used to calculate R _G from data ( n = 68) from a doubly labelled water study of free-ranging Garter Snakes ( Thamnophis sirtalis fitchi ) in northern California.
3. The sample-wise ('ecological') cost of growth was 2·07 kJ per gram of net growth (equivalent to 8·63 kJ g^–1 dry tissue); reanalysis of a subset of efficient growers yielded a more conservative 'physiological' estimate of 1·67 kJ g^–1.
4. Our empirical estimate of R _G, among the first reported for squamate reptiles and free-living animals of any kind, compares closely with published, laboratory-derived values for ectotherms.
5. The metabolic costs of growth accounted for an average of 30% of total field metabolic rates for these snakes, which were growing at a mean rate of 3% of body mass per day. However, our method probably underestimated the total ecological cost of growth for large animals, because potential growth costs that covary with body size were not included.
6. Distinction between conceptual and empirical energy budgets clarifies relationships among body size, metabolic rates, and the physiological and ecological costs of growth.