Towards an understanding of symbiont natural history through studies of crayfish and their annelid associates

Crayfish throughout North America, Europe, and Asia host assemblages of obligate ectosymbiotic annelid worms called branchiobdellidans. The work presented here is a detailed experimental and observational study of the ecological interactions between crayfish and their worms. In a comprehensive literature review, I show that branchiobdellidans have complex and context-dependent effects on their hosts, serving as both beneficial cleaners and tissue-consuming parasites. Using a field survey and laboratory experiments, I provide novel evidence for age-specific resistance as an adaptation to maximize life-long benefits of a mutualism. Specifically, I show that Cambarus crayfish display a consistent ontogenetic shift in resistance to the colonization of branchiobdellidans and this shift likely reflects underlying changes in the costs and benefits of symbiosis. I then show that this change in host resistance creates predictable patterns of symbiont diversity and composition throughout host ontogeny. Host resistance limits within-host symbiont communities to a few weakly interacting species, whereas relaxed resistance leads to more diverse symbiont communities that have strong interactions among symbiont taxa. Thus, host resistance has direct effects on within-host symbiont community structure by selectively filtering colonizing species, and indirect effects by moderating the strength of interactions among symbionts. Lastly, in a detailed study of the worm Cambarincola ingens, I depict a symbiont dispersal strategy that yields highly predictable transmission dynamics during pairwise host-host encounters and shows that variation in transmission dynamics can be explained by the fitness outcomes for dispersing symbionts. Field observations revealed that worm reproduction is contingent on host size and intraspecific competition for preferred microhabitats. Using a predictive model that assumes transmission of symbionts only when current conditions yield fitness below a minimum threshold, I was able to predict individual transmission events much more accurately than a comparable null model that assumed a fixed probability of transmission. My work provides empirical support for the emerging trend among researchers that advocates the adaptation of general ecological frameworks to understand symbiont population structure and diversity, but my work also emphasizes the value of detailed natural history studies to uncover system-specific ecological and co-evolutionary processes such as partner control mechanisms, symbiont microhabitat selections, and symbiont dispersal strategies.