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I am interested in the interrelationships among natural products chemistry, behavioral biology, reproductive endocrinology, and ecology. I use a comparative, interdisciplinary approach that combines and integrates the molecular, organismal, and ecological levels of analysis. My research is conducted both in the laboratory and in the field in order to elucidate the role of hormones and pheromones in orchestrating reproductive behaviors and physiology. Field and laboratory studies are complementary, bridging the gap between biochemistry and behavioral ecology by incorporating laboratory-based analyses of the structure, manufacture, and delivery of hormones or pheromones, with studies of the animal's physiological ecology and behavior in the field. Thus, my research questions are most applicable to three areas of specialization: chemical ecology, behavioral ecology, and behavioral endocrinology.
Reptiles are excellent vertebrate models for chemical ecology research because they rely more on their chemical senses than any other vertebrate class. I have found that snakes present bioassays that are robust, simple to quantify, and unequivocal since they are context-specific. Specifically, reproduction in snakes seems to be dependent on the production and perception of sex pheromones. One question we are examining is how chemical communication systems evolved in vertebrates by examining both the diversity of chemical signals and the underlying physiological and endocrinological mechanisms involved in their production and expression. For example, using state-of-the- art chemical techniques such as gas chromatography/mass spectrometry and nuclear magnetic resonance spectroscopy, we have isolated, identified, and synthesized the first pheromone in a reptile, the red-sided garter snake, Thamnophis sirtalis parietalis. My students and I conducted field studies that investigated the role of these pheromones at the population level and discovered that a small subset of males mimic the female pheromones, perhaps gaining a selective advantage in mating. We discovered that these female mimics are using aromatase enzymes in their skin to convert androgens to estrogens and thus promote the production and expression of the female sex pheromones in their skin. Recent work with my collaborator, Rick Shine, now indicates that many of the males may be producing the female sex attractiveness pheromones in order to warm up faster after emergence from hibernation and avoid predation.
Pheromones are thought to be potent reproductive isolating mechanisms. Along with my former student, Mike LeMaster (Asst. Professor, Western Oregon University), we have been exploring the role of variation in the sex attractiveness pheromone system of the red-sided garter snake. We now know that with a single tongue-flick, a male garter snake can determine not only whether another snake is a member of its own species, but also if it is a male or female, a female from the male’s own den versus another den, a large female versus a small female (larger females produce more young), and whether a female is likely to reproduce this year or store his sperm for a following year. We are now expanding these studies to investigate a syntopic congener, the Western plains garter snake, Thamnophis radix, and an allotopic conspecific, the red-spotted garter snake, Thamnophis sirtalis concinnus here in Oregon.
Our behavioral ecology studies have greatly benefited from collaborations with other senior scientists. Rick Shine of the University of Sydney, Australia, and I have been working together for the past 6 years on garter snakes in Manitoba, and recently, sea snakes in Vanuatu and New Caledonia. Our work on the garter snakes has examined fundamental questions such as male body size and mating success, size-assortative mating, mating plugs, female mimicry, antipredator tactics, thermoregulatory behavior, migratory behavior and others. This work has been very productive and is ongoing. Another more recent collaboration involves Steve Arnold of OSU and Mike Pfrender of Utah State University. They, along with my students and I, are investigating the mechanisms by which female choice operates in this model species. We hypothesize that females may not be able to choose a particular male out of her hundreds of suitors; however, she may be able to choose how many times she mates. Thus, we are investigating the phenomenon of multiple mating, paternity analyses, and sperm competition in this species. One of my current students, Ryan O’Donnell, is using trailing behavior as a powerful behavioral indicator. He has been studying the ability of male garter snakes to distinguish trails of mated females from those of unmated females. The evolutionary consequences of these choices makes for an interesting study. He is also looking at the ontogenetic shift in male garter snakes from mating behavior to feeding behavior. These behaviors are almost mutually exclusive in the red-sided garter snake and Ryan is investigating the fundamental control mechanisms.
Our behavioral endocrinology work has mostly focused on the role of steroid hormones and their mediation of reproductive behaviors and physiology. My former student, Ignacio Moore (Post-doc, University of Washington), investigated the interaction of stress and reproduction. Most animals when stressed will produce and express glucocorticoids. These steroid hormones serve to mobilize energy stores for use in combating the stressor. One of the additional effects of glucocorticoid release is the suppression of reproduction in terms of gonadal steroid production and gamete production. However, there are some animals that live in extreme environments that do not follow this classical paradigm. Ignacio conducted comparative work on the reproductive physiology of Oregon garter snakes and Manitoba garter snakes and showed that the Manitoba snakes are unique in being able to partially suppress their stress response and still exhibit sexual behavior. The Oregon snakes’ reproduction was completely suppressed in response to an identical stressor. My most recent Ph.D. student, Deborah Lutterschmidt, investigated the role of melatonin in synchronizing reproductive behavior and physiology with rising and falling temperature cues, not photoperiodic cues, as is the norm in other vertebrates. In the red-sided garter snake, hibernation occurs for 8 months underground; therefore, photoperiodic cues have no role in modulating reproduction in this species.
At an applied level, my laboratory was actively involved in attempting to utilize pheromones as a means of biological control. Our research on the introduced pest species, the brown tree snake, Boiga irregularis, serves to demonstrate the utility of sex pheromones as attractants and repellents. The brown tree snake of Guam is an introduced pest species that has extirpated 13 species of birds, attacked human infants, and is responsible for millions of dollars of damage to power generating equipment on Guam. My former student, Mike Greene (Asst. Professor, Univ. Colorado, Denver), described the sex behavior and combat behaviors of this species and how they are mediated by pheromones. These studies were conducted in both the laboratory and the field. My last student that worked on this, Heather Waye, conducted the field work in Guam while an additional ongoing project looking at the brown tree snake in its native range, Australia and New Guinea, was conducted with a long-time collaborator, Joan Whittier, of the University of Queensland. This work holds great promise and if successful, it will be the only example of pheromonal control of a vertebrate pest species.