Discovery of indirect parasite life cycles at deep-sea hydrothermal vents

Deep-sea hydrothermal vents are extreme, isolated, and ephemeral ecosystems populated by unique endemic fauna, making them a potentially challenging setting for the survival of parasites with indirect (multi-host or ‘complex’) life cycles. We examined the animal communities at a frequently disturbed hydrothermal vent field (9°50’N, East Pacific Rise) to explore whether parasites with indirect life cycles complete their life cycles within this island-like, ephemeral marine habitat, which has been previously hypothesized but is not known. Our dissections of individuals from 51 vent species revealed 7 morphogroups of parasitic flatworms (trematodes) including the genera Biospeedotrema, Caudotestis, and Neolebouria, and 4 life stages in the multi-host trematode life cycle. Adult trematode life stages lived in the vent fishes Thermarces cerberus and Thermichthys hollisi, while the intermediate life stages were found in a variety of crustacean, gastropod, and polychaete species. Genetic barcoding of the 18S, 28S, and ITS2 regions linked sequential life stages for some of the morphogroups, revealing the phylogenetic position and routes of transmission between hosts for vent trematodes. This study provides the most direct evidence yet that parasites very likely complete indirect life cycles in deep-sea hydrothermal vent ecosystems, with important implications for the persistence and diversity of parasites in disturbed environments.