Neil B. Ford

Phenotypic Plasticity in Reproductive Traits: Evidence from a Viviparous Snake

A number of recent studies have indicated that life history characteristics (e.g., number of offspring, offspring size, age at sexual maturity) are strongly affected by proximate environmental factors such as prey availability. Evaluating this phenotypic plasticity will be crucial to a complete understanding of the evolution of life history traits, because the occurrence of such variability casts doubt on the common assumption that the values of life history characteristics expressed in nature are the outcome of long-term natural selection. In this study, we manipulated the diets of a captive-bred colony of the viviparous snake Thamnophis marcianus to determine to what degree the reproductive characteristics of this species were determined by food intake. We found that both number of offspring and clutch mass were significantly affected by prey availability, but that relative clutch mass and offspring size were fixed relative to diet. Our data suggest that like other organisms, T. marcianus shows a gradient in phenotypic plasticity, with some traits more canalized than others. Therefore, intraspecific comparisons of life history characteristics should not be made without information on which traits are subject to phenotypic plasticity.

THE ROLE OF PHEROMONE TRAILS IN THE SOCIOBIOLOGY OF SNAKES

In his review of reptilian social systems, Brattstrom (1974) stated that “nobody has, in my opinion, designed the appropriate experiments to study social behavior in snakes properly.” In the subsequent decade, studies of snake behavior have proliferated, but Brattstrom’s comments regarding studies of snake sociobiology are essentially still true. Most reports remain observational accounts and descriptions of ritualistic behaviors involved in reproductive and agonistic encounters (reviewed by Carpenter, 1977; Carpenter and Ferguson, 1977). Very few biologists have attempted to experimentally examine the sociobiological functions of such displays. However, for a good example, see Gillingham et al.’s (1983) test of courtship activity of male diamondback rattlesnakes (Crotalus atrox), after combat dances.

Trophic and maternal transfer of selenium in brown house snakes (Lamprophis fuliginosus)

Excessive concentrations of dietary Se are toxic to oviparous vertebrates (i.e., fish and birds) but little is known about its accumulation and effects in reptiles. We exposed female brown house snakes, Lamprophis fuliginosus, to 10 and 20 microg/g Se by injecting seleno-D,L-methionine into their prey items and compared the snakes to individuals receiving background levels of approximately 1 microg/g dietary Se. Snakes were fed meals equaling 25% of their body mass 2-3 times a month for 10 months. Snakes exposed to excessive Se accumulated significant concentrations of Se in kidney, liver, and ovarian tissue, but accumulation had no effect on female survival, food consumption, growth, or body condition. Fewer females exposed to excessive Se reproduced than females exposed to 1 microg/g Se (67% vs. 91%, respectively), but the reduction in reproductive activity was not statistically significant. Total reproductive output of females did not differ among the three dietary treatments. However, snakes exposed to 10 and 20 microg/g Se transferred significant concentrations of Se to their eggs. In the 20 microg/g treatment, maternal transfer resulted in Se concentrations in eggs that surpassed all suggested reproductive toxicity thresholds for birds and fish. Further studies are needed to more rigorously determine whether maternal transfer of Se in this snake species affects the viability of developing embryos or the health of offspring.

Sex pheromone source location by garter snakes: : A mechanism for detection of direction in nonvolatile trails.

Male plains garter snakes,Thamnophis radix, tested in a 240-cm-long arena can detect directional information from a female pheromone trail only when the female is allowed to push against pegs while laying the trail. The females normal locomotor activity apparently deposits pheromone on the anterolateral surfaces of vertical structures in her environment. The male sensorily assays the sides of these objects and from this information determines the females direction of travel.

Male red-sided garter snakes, Thamnophis sirtalis parietalis, determine female mating status from pheromone trails

Recently mated females of some species experience a refractory period following mating during which a physiological change or a mating plug prevents remating. Males that determine female mating status from a distance will minimize time spent searching for mates by avoiding unavailable females. Female redsided garter snakes experience a refractory period after mating due to a mating plug. Female garter snakes leave pheromone trails, which males detect and follow to find potential mates. We investigated the ability of male garter snakes to determine the mating status of females based solely on these pheromone trails. Males were given a choice between following two trails on a Y maze to examine whether they discriminate between mated and unmated females, whether this discrimination is based on changes in the sexattractiveness pheromone or the copulatory fluids, and whether they continue to discriminate after the mated females have lost their mating plug. We found that male garter snakes discriminate between the trails of mated and unmated females. This discrimination is based on the presence of a copulatory pheromone, rather than changes in the sex-attractiveness pheromone. The duration of the copulatory pheromone coincides with the duration of the mating plug. Thus, male garter snakes are able to minimize time spent searching for unavailable females by determining female mating status from a distance.

Courtship of the garter snake, Thamnophis marcianus, with a description of a female behavior for coitus interruption

Since Gillinghams (1974, 1976, 1977) original works on the breeding behavior of snakes, additional studies have utilized his triphasic model in a variety of snake species (Ford, 1982; Gillingham et al., 1977; Gillingham and Chambers, 1982; Gillingham et al., 1983; Hayes, 1986; Murphy and Barker, 1980; Secor, 1987). However, no such analysis has been applied to the courtship patterns of any species of thamnophine snake. This study catalogues the courtship behavior pattern of the checkered garter snake, Thamnophis marcianus, using a modified version of Gillinghams (1976) male motor patterns. Adult T. marcianus originally collected from La Salle County, Texas, were individually housed in an animal room at the University of Texas at Tyler which ranged from 26-30 C with a photoperiod of 12L:12D. Water was available at all times and the snakes were fed

The role of insulin-like growth factor-1 (IGF-1) in growth and reproduction in female brown house snakes (Lamprophis fuliginosus)

Insulin-like growth factor-1 (IGF-1) is a peptide hormone critically involved in the regulation of key life-history traits such as growth and reproduction. Its structure and function are well-characterized among diverse mammal, fish, and bird species; however, little is known regarding the activities of IGF-1 in non-avian reptiles, particularly snakes and lizards. Nevertheless, several unique characteristics of reptiles, such as high metabolic flexibility and remarkable diversity in life-history strategy, suggest that they are of great interest in the study of endocrinological mechanisms underlying the regulation and evolution of life-history traits. Here we test for a relationship between IGF-1 and individual feeding rate, growth rate and reproductive stage in lab-reared female offspring of wild-caught oviparous house snakes, Lamprophis fuliginosus. We confirm a positive correlation between IGF-1 and both feeding and growth rates in sexually immature snakes, similar to that reported in other taxa. We also show a family effect on IGF-1, suggesting that IGF-1 levels may be heritable in these snakes, and serve as an important target of selection to produce divergent life-history strategies. Furthermore, we provide evidence that suggests that IGF-1 may peak rapidly after first mating, and subsequently decline prior to egg-laying, a phenomenon not previously reported in other taxa. These findings suggest that further comparative study of IGF-1 in snakes may reveal both the extent to which IGF-1 function is conserved across major taxonomic groups, as well as novel and intriguing roles for IGF-1 in the regulation of reproductive activities.

Rates of molecular evolution vary in vertebrates for insulin-like growth factor-1 (IGF-1), a pleiotropic locus that regulates life history traits.

Insulin-like growth factor-1 (IGF-1) is a member of the vertebrate insulin/insulin-like growth factor/relaxin gene family necessary for growth, reproduction, and survival at both the cellular and organismal level. Its sequence, protein structure, and function have been characterized in mammals, birds, and fish; however, a notable gap in our current knowledge of the function of IGF-1 and its molecular evolution is information in ectothermic reptiles. To address this disparity, we sequenced the coding region of IGF-1 in 11 reptile species-one crocodilian, three turtles, three lizards, and four snakes. Complete sequencing of the full mRNA transcript of a snake revealed the Ea-isoform, the predominant isoform of IGF-1 also reported in other vertebrate groups. A gene tree of the IGF-1 protein-coding region that incorporated sequences from diverse vertebrate groups showed similarity to the species phylogeny, with the exception of the placement of Testudines as sister group to Aves, due to their high nucleotide sequence similarity. In contrast, long-branch lengths indicate more rapid divergence in IGF-1 among lizards and snakes. Additionally, lepidosaurs (i.e., lizards and snakes) had higher rates of non-synonymous:synonymous substitutions (dN/dS) relative to archosaurs (i.e., birds and crocodilians) and turtles. Tests for positive selection on specific codons within branches and evaluation of the changes in the amino acid properties, suggested positive selection in lepidosaurs on the C domain of IGF-1, which is involved in binding affinity to the IGF-1 receptor. Predicted structural changes suggest that major alterations in protein structure and function may have occurred in reptiles. These data propose new insights into the molecular co-evolution of IGF-1 and its receptors, and ultimately the evolution of IGF-1s role in regulating life-history traits across vertebrates.

Ontogenetic and sexual differences in diet in an actively foraging snake, Thamnophis proximus

Actively foraging species of snakes often consume large numbers of small prey, which creates a high meal to snake mass ratio. Because they may also rely on speed to avoid predation, this might negatively influence survival. We examined the diet of 313 western ribbon snakes (Thamnophis proximus Say in James, 1823), a very attenuated species, in a floodplain in northeastern Texas. Of the 142 individuals with food, adult males ate 9 prey types, followed by females with 8, and juveniles only 6. The ontogenetic increase in prey diversity was predicted. However, female ribbon snakes are larger than males and their fewer prey types may reflect a strategy where smaller prey are dropped from the diet. Seasonal activity of prey and snake class was generally correlated. Overall individual prey sizes were comparably small. However, over 50% of the snakes contained multiple prey and total meal masses were similar to the maximum prey sizes of ambush foragers. Adults stopped feeding at proportionally lower meal mass to ...

Courtship and mating behavior in the brown house snake Lamprophis fulginosus

Courtship behavior in snakes may serve several roles, including species identification, timing of gamete production, and evaluation of fitness of the partner (Ford and Burghardt, 1993). The behavioral acts involved in species identification could be of potential use in taxonomy and systematics (Secor, 1987). However, most accounts of mating in snakes are qualitative and lack descriptions that are sufficiently accurate to examine species specific traits. The most useful descriptions of courtship patterns for evolutionary comparisons utilize sequence analysis of the data (Gillingham, 1987) and for snakes those reports are limited to Elaphe (Gillingham, 1979), Lampropeltis (Secor, 1987), Agkistrodon (Schuett and Gillingham, 1988), and Thamnophis (Rossman et al., 1996). In this paper, we describe the courtship behavior of the brown house snake, Lamprophis fulginosus, a wide-spread south African colubrid snake of the subfamily Boodontinae and compare it to the courtship behavior described for other colubrids.