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Social organization in trematode parasitic flatworms

Abstract

As in the most complex animal societies, trematodes (parasitic flatworms) live in colonies characterized by a high degree of cooperative organization. My research started with the unexpected observation that several trematode species have a reproductive division of labor with morphologically and behaviorally distinct reproductive and non-reproductive castes. The non-reproductive individuals are smaller but have relatively large mouthparts. They are more active than their reproductive counterparts and disproportionately common in areas of the host where invasions by other trematodes occur. Finally, only non-reproductive individuals readily attack enemies with their mouths. Thus, it is clear that one major role of these individuals is to defend the colony from enemy trematode invaders; they are soldiers.

The initial discovery was followed by reports revealing the existence of soldiers in five additional trematode species and by research examining the adaptive significance of soldiers. However, descriptions of colony structure were restricted to a single trematode superfamily (Echinostomatoidea), and knowledge of colony demography and caste function was limited to snapshots of the condition of mature colonies. My doctoral dissertation has laid the foundation to explore the evolution of this remarkable social organization in trematodes, as well as the mechanisms regulating it.

Here I quantify morphology, distribution, and behavior of parasites from both establishing and fully developed colonies of sixteen species of trematodes that infect the California horn snail. While showing that eight additional species have a soldier caste, including four species from a new superfamily, I expand the phylogenetic range for which trematode sociality has been examined. I identify patterns underlying colony structure for trematode species that lack a soldier caste and establish discrete criteria to recognize colonies with and without soldiers. Finally, I develop an in vitro system for cultivation of marine trematodes that includes co-culture with Biomphalaria glabrata embryonic (Bge) cell line and media with Bge-released factors. The results presented here highlight the promise of these methods to address questions regarding trematode sociality, interspecific interactions, development and caste differentiation.

Trematode colonies are readily replicated, can be maintained in large numbers, and are amenable to in vitro studies. Hence, they provide many advantages as model systems to pursue experimental and comparative research probing general principles underlying the ecology and evolution of sociality. Furthermore, there are more than 20,000 species of trematodes worldwide. They cover a wide range of environmental and life history diversity and are both ecologically and medically important. Thus, understanding the mechanisms that shape trematode communities can have substantial public health, veterinary and wildlife disease applications.

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