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Reproductive Implications of Parasitic Infections and Immune Challenges in Garter Snakes

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Reproductive Implications of Parasitic Infections and Immune Challenges in Garter Snakes AN ABSTRACT OF THE DISSERTATION OF Emily J. Uhrig for the degree of Doctor of Philosophy in Zoology presented on April 21, 2015. Title: Reproductive Implications of Parasitic Infections and Immune Challenges in Garter Snakes Abstract approved: ______________________________________________________ Robert T. Mason Parasitic infections and immune challenges can affect host reproductive fitness and, ultimately, the evolution of host populations in a myriad of ways. The fitness implications of parasitic infections range from increased host mortality to subtle changes in reproductive investment. From alterations of behaviors, sexual signaling, and competitive ability to changes in gamete production and fertilization success, it is clear that parasites are capable of mediating sexual selection and influencing host reproductive fitness even without altering mortality. The mechanisms underlying fitness effects highlight the complexity of the host-parasite relationship which involves immune responses as well as a range of other, often interactive, physiological processes within the host. In some instances, it is not the direct effect of parasites per se, but rather the hosts’ responses to infection that mediate fitness consequences. This dissertation presents studies designed to elucidate the implications of parasitism and immune responses for the reproductive fitness of garter snakes (genus Thamnophis). In chapter 2, “Alaria mesocercariae in the tails of red-sided garter snakes: evidence for parasite-mediated caudectomy”, I focus on the histopathological changes associated with a trematode (Alaria sp.) infecting the tails of red-sided garter snakes (T. sirtalis parietalis). My results demonstrate that Alaria mesocercariae occur in high density within the tail tissue of both male and female snakes with as many as 2,000 mesocercariae in a single tail; infection prevalence was 100% in the snakes I examined. I found no evidence of intersexual variation in pathological changes or infection densities. For both sexes, external pathological manifestations include swelling of the tail while, internally, the aggregation of mesocercariae leads to the formation of mucus-filled pseudocysts and damage of muscle tissue. In severe cases, the extent of tissue destruction appeared to weaken the connection of the tail to the rest of the body, a condition that would facilitate tail breakage, which in turn negatively affects the snake’s fitness by impairing mating success. From the parasite’s perspective, tail breakage is likely beneficial by facilitating its transmission to subsequent hosts in its life cycle. Alaria sp. are not the only parasites commonly infecting garter snakes and in chapter 3, “Patterns in parasitism: interspecific and interpopulational variation in helminth assemblages and their reproductive fitness correlates in garter snakes”, I broaden our investigation to include a suite of helminth parasites common in the garter snakes of Manitoba, Canada. My results demonstrate that helminth assemblages of two garter snake species (red-sided garter snakes, T. sirtalis parietalis, and plains garter snakes, T. radix) include Lechriorchis trematodes and Rhabdias nematodes in the lung, Alaria mesocercariae in the tail, and diplostomid trematode metacercariae in the visceral fat; red-sided garter snakes also had gastrointestinal cestodes. Helminth assemblages varied, mainly in terms of parasite density, among populations of red-sided garter snakes and between red-sided and plains garter snakes, but it is unclear whether this variation is due simply to diet-based differences in parasite exposure or whether variation in parasite resistance may have a role. Notably, for plains garter snakes and one red-sided garter snake population I found helminth densities to be predictive of male fitness correlates, namely body condition, testes mass, and sperm counts. Thus, parasitism in garter snakes clearly has important implications for reproductive fitness beyond just influencing tail loss. These results highlight the importance of considering more than a single parasite or single fitness correlate when exploring host-parasite relationships. The consequences of parasitic infections may arise simply through the activation of the host’s immune system rather than the presence of parasites. Thus, in chapter 4, “Changes in reproductive investment and hormone levels in response to an acute immune challenge”, I use lipopolysaccharide (LPS) to assess immune-reproductive tradeoffs of male red-sided garter snakes during the breeding season. As LPS is non-pathogenic, I was able to assess the fitness implications of the immune activation itself. My results showed that males depress courtship behaviors and mating success when faced with a single acute immune challenge. For LPS-treated males that did mate, copulatory plug mass was significantly lower compared to controls, while sperm counts did not differ between treatments. This result likely reflects the dissociated breeding pattern of these snakes as spermatogenesis occurs outside the breeding season and, thus, sperm stores were already in place prior to the immune challenge whereas plug material is produced during the breeding season. Further, the LPS treatment was correlated with increased plasma levels of corticosterone, which were 1.8 times higher in LPS-treated males compared to controls, and decreased levels of androgens, which, in LPS-treated males, were only one third as high as androgen levels in control males. Thus, the observed immune-reproduction tradeoff appeared to be hormonally-mediated. Indeed, the low breeding season androgen levels characteristic of this dissociated breeder may have relaxed testosterone-mediated immunosuppression and so facilitate immune-induced suppression of reproductive behaviors. The results of this study highlight the influence of host life history on the consequences of immune activation and also emphasize the complex interactions between the immune, reproductive and endocrine systems. In chapter 5, “Implications of repeated immune challenges in a capital breeder with prolonged hibernation”, I again utilized LPS as a means of investigating the implications of immune activation. In this study, I administered a series of LPS injections to male and mated female snakes throughout the summer feeding season, and, for males, into the autumn. Females give birth during the summer and males undergo testicular recrudescence and spermatogenesis during summer and into autumn so these seasons represent important reproductive periods for red-sided garter snakes. Also, as capital breeders, it is during the summer feeding season that snakes of both sexes accumulate the resources upon which they will rely throughout hibernation and the subsequent breeding season. For the most part, my results did not demonstrate clear immune-reproductive tradeoffs. It appears that the absence of tradeoffs may be due to immune-challenged males and gravid female compensating for the immune challenge and maintaining reproductive processes by increasing their food intake, which was not limited during the study. Indeed, LPS-treated gravid females actually had more offspring per litter compared to gravid control females, suggesting that the immune challenge led to greater investment in offspring. In contrast to gravid females, non-gravid females treated with LPS exhibited reduced food intake which may reflect a survival strategy as anorexia during infections tends to be beneficial for survival. Interestingly, the increased food consumption of males did not translate into greater fat stores, but rather higher liver masses which may be indicative of immunopathological changes which should be explored in future studies. ©Copyright by Emily J. Uhrig April 21, 2015 All Rights Reserved Reproductive Implications of Parasitic Infections and Immune Challenges in Garter Snakes by Emily J. Uhrig A DISSERTATION submitted to Oregon State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Presented April 21, 2015 Commencement June 2015 Doctor of Philosophy dissertation of Emily J. Uhrig presented on April 21, 2015 APPROVED: Major Professor, representing Zoology Chair of the Department of Integrative Biology Dean of the Graduate School I understand that my dissertation will become part of the permanent collection of Oregon State University libraries. My signature below authorizes release of my dissertation to any reader upon request. Emily J. Uhrig, Author ACKNOWLEDGEMENTS To my mom and dad, and Uncle Donald for enduring support and encouragement of a waterdog girl. CONTRIBUTION OF AUTHORS For Chapter 2: E. J. Uhrig developed the initial study design, collected and preserved all tissue samples, conducted non-histological lab work, conducted all statistical analyses, and wrote the majority of the manuscript. S. T. Spagnoli prepared histological slides and histology images, contributed to the corresponding methods section and provided histopathological descriptions for the results. M. L. Kent assisted with study design and R. T. Mason assisted with animal collection. For Chapters 3, 4, and 5: E.J. Uhrig designed the studies, performed dissections, collected data and processed sperm samples, conducted all statistical analyses and wrote the manuscript. C.R. Friesen and L. A. Blakemore assisted with data collection. R. T. Mason assisted with animal collection. For chapter 4, D. I. Lutterschmidt collected blood samples and conducted radioimmunoassays. TABLE OF CONTENTS Page CHAPTER1: GENERAL
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