Ecoimmunological Investigations of the Cottonmouth (Agkistrodon piscivorus)

Abstract

Despite the benefits gained from studying the immune system of non-traditional model organisms, including the discovery of key components of the human immune system, squamates remain the most poorly-understood major vertebrate group in terms of immune system components and function. This bias is more striking given that squamates may play important roles in disease transmission cycles; without even a rudimentary understanding of susceptibility and infection clearance in these vertebrates, transmission models will be incomplete. This dissertation explores the following areas: 1) thermal biology of innate immune (complement) function in snakes; 2) seasonal endocrine/immune patterns in free-living snakes; 3) endocrine/immune differences between pregnant and non-pregnant snakes; and 4) the seasonal pattern of exposure to eastern equine encephalitis virus (EEEV) in amphibians and reptiles from Tuskegee National Forest in Alabama. These studies focused on wild-living cottonmouths (Agkistrodon piscivorus), a large-bodied snake often found in high densities that experiences infection with arthropod-borne viruses (e.g., EEEV). Complement system function of cottonmouths exhibits a positive correlation with experimental temperature, such that the plasma’s ability to lyse bacteria is maximal at temperatures above the range experienced by cottonmouths in the wild. However, seasonal variation in complement performance does not appear to be associated with seasonal variation in cottonmouth body temperatures, body condition, or patterns of steroid hormone secretion and reproduction. Given the repeated demonstration of immune modulation during pregnancy in unrelated vertebrates, I predicted and confirmed a difference in complement performance between pregnant and non-pregnant females, and this was negatively correlated with the sex steroid progesterone. These findings suggest that, although certain features of vertebrate functional immunity appear to be conserved or convergent among ectotherms (e.g., immune modulation during pregnancy), the overarching influence of body temperature on ectothermic immune systems constitutes a substantial functional difference among vertebrates. As this difference may influence transmission patterns of arthropod-borne viruses with broad host ranges, the seasonal prevalence of EEEV exposure in cottonmouths and other terrestrial ectotherms, and the results support a role for squamates—specifically snakes—as underappreciated arbovirus reservoirs and overwintering hosts.