The most vagile host as the main determinant of population connectivity in marine macroparasites

Although molecular ecology of macroparasites is still in its infancy, general patterns are beginning to emerge, e.g. that the most vagile host in a complex life cycle is the main determinant of the population genetic structure of their parasites. This insight stems from the observation that populations of parasites with only freshwater hosts are more structured than those with terrestrial or airborne hosts. Until now, the same has not been tested for marine systems, where, in theory, a fully marine life cycle might sustain high dispersal rates because of the absence of obvious physical barriers in the sea. Here, we tested whether a marine trematode parasite that utilises migratory birds exhibited weaker population genetic structure than those whose life cycle utilises marine fish as the vagile host. Part of the mitochondrial cytochrome c oxidase 1 (COI) gene was sequenced from individual sporocysts from populations along the Atlantic coast of Europe and North Africa. Strong population structure (Φst = 0.25, p < 0.0001) was found in the fully marine trematode Bucephalus minimus (hosted by fish), while no significant structure (Φst = 0.015, p = 0.19257) was detected in Gymnophallus choledochus (hosted by birds). However, demographic models indicate recent colonisation rather than high dispersal as an alternative explanation of the low levels of structure observed in G. choledochus. Our study is the first to identify significant genetic population structure in a marine autogenic parasite, suggesting that connectivity between populations of marine parasites can be limited despite the general potential for high dispersal of their hosts in the marine environment.