Charles F. Smith

Facultative parthenogenesis discovered in wild vertebrates

Facultative parthenogenesis (FP)—asexual reproduction by bisexual species—has been documented in a variety of multi-cellular organisms but only recently in snakes, varanid lizards, birds and sharks. Unlike the approximately 80 taxa of unisexual reptiles, amphibians and fishes that exist in nature, FP has yet to be documented in the wild. Based on captive documentation, it appears that FP is widespread in squamate reptiles (snakes, lizards and amphisbaenians), and its occurrence in nature seems inevitable, yet the task of detecting FP in wild individuals has been deemed formidable. Here we show, using microsatellite DNA genotyping and litter characteristics, the first cases of FP in wild-collected pregnant females and their offspring of two closely related species of North American pitviper snakes—the copperhead (Agkistrodon contortrix) and cottonmouth (Agkistrodon piscivorus). Our findings support the view that non-hybrid origins of parthenogenesis, such as FP, are more common in squamates than previously thought. With this confirmation, FP can no longer be viewed as a rare curiosity outside the mainstream of vertebrate evolution. Future research on FP in squamate reptiles related to proximate control of induction, reproductive competence of parthenogens and population genetics modelling is warranted.

Mating systems, reproductive success, and sexual selection in secretive species: a case study of the western diamond-backed rattlesnake, Crotalus atrox.

Long-term studies of individual animals in nature contribute disproportionately to our understanding of the principles of ecology and evolution. Such field studies can benefit greatly from integrating the methods of molecular genetics with traditional approaches. Even though molecular genetic tools are particularly valuable for species that are difficult to observe directly, they have not been widely adopted. Here, we used molecular genetic techniques in a 10-year radio-telemetric investigation of the western diamond-backed rattlesnake (Crotalus atrox) for an analysis of its mating system and to measure sexual selection. Specifically, we used microsatellite markers to genotype 299 individuals, including neonates from litters of focal females to ascertain parentage using full-pedigree likelihood methods. We detected high levels of multiple paternity within litters, yet found little concordance between paternity and observations of courtship and mating behavior. Larger males did not father significantly more offspring, but we found evidence for size-specific male-mating strategies, with larger males guarding females for longer periods in the mating seasons. Moreover, the spatial proximity of males to mothers was significantly associated with reproductive success. Overall, our field observations alone would have been insufficient to quantitatively measure the mating system of this population of C. atrox, and we thus urge more widespread adoption of molecular tools by field researchers studying the mating systems and sexual selection of snakes and other secretive taxa.

Biological Inquiry: A New Course and Assessment Plan in Response to the Call to Transform Undergraduate Biology

We transformed our first-year curriculum in biology with a new course, Biological Inquiry, in which >50% of all incoming, first-year students enroll. The course replaced a traditional, content-driven course that relied on outdated approaches to teaching and learning. We diversified pedagogical practices by adopting guided inquiry in class and in labs, which are devoted to building authentic research skills through open-ended experiments. Students develop core biological knowledge, from the ecosystem to molecular level, and core skills through regular practice in hypothesis testing, reading primary literature, analyzing data, interpreting results, writing in disciplinary style, and working in teams. Assignments and exams require higher-order cognitive processes, and students build new knowledge and skills through investigation of real-world problems (e.g., malaria), which engages students’ interest. Evidence from direct and indirect assessment has guided continuous course revision and has revealed that compared with the course it replaced, Biological Inquiry produces significant learning gains in all targeted areas. It also retains 94% of students (both BA and BS track) compared with 79% in the majors-only course it replaced. The project has had broad impact across the entire college and reflects the input of numerous constituencies and close collaboration among biology professors and students.

Reproduction in female copperhead snakes (Agkistrodon contortrix): plasma steroid profiles during gestation and post-birth periods.

We investigated levels of plasma progesterone (P4), 17&bgr;-estradiol (E2), testosterone (T), and corticosterone (CORT) during gestation and post-birth periods in wild-collected female copperhead snakes (Viperidae; Agkistrodon contortrix). We also sought to determine whether CORT levels at (or near) birth dramatically increase and were correlated with duration of labor and litter size. Specifically, pregnant subjects (N = 14) were collected during early- to mid-gestation, held in the laboratory, and repeatedly bled to obtain plasma for steroid analyses. Progesterone showed significant changes during gestation, with the highest levels at the onset of sampling (circa 50 days prior to birth); P4 progressively declined up to parturition, and basal levels were observed thereafter. At the onset of sampling, E2 was at peak levels and fell sharply at circa 30 days prior to birth, a trend observed throughout the post-birth sampling period. Throughout the entire sampling period, T was undetectable. Although CORT showed no significant changes during gestation and several days following parturition, there was a highly significant peak at the time of birth. Our findings mirror the results of previous studies on pregnancy and steroid hormones of other live-bearing snakes, lizards, and mammals. As expected, there was a significant relationship between duration of labor and litter size; however, although levels of CORT did not achieve significance, there was a positive trend with litter size. We suggest that elevation of CORT at birth is involved in the mobilization and regulation of energy stores necessary for the physiological process of parturition and as a possible mechanism to trigger birth.

Putative Pair-Bonding in Agkistrodon contortrix (Copperhead)

Abstract Pair-bonding between sexes is common in vertebrate taxa, yet it has been noted far less frequently in some groups such as reptiles, and snakes in particular. Evidence to date indicates that many snake mating-systems are polyandrous, with both males and females having multiple partners in a single breeding season, and thus unlikely to exhibit lengthy pair-bonds. Wittenberger and Tilson (1980) suggested that pair-bonding exists when pairs remain intact for a consecutive period equaling at least 25% of the breeding season. Using this criterion, we present evidence of pair-bond formation in a North American pitviper, Agkistrodon contortrix (Copperhead), a species with a polyandrous mating system.