Evolution in a multi-host parasite: Chronobiological circadian rhythm and population genetics of Schistosoma japonicum cercariae indicates contrasting definitive host reservoirs by habitat

Schistosomiasis japonica is a disease of profound medical and veterinary importance which has remained endemic in many regions and has re-emerged where previously controlled in China. Although over 40 mammalian species are suspected as reservoirs for Schistosoma japonicum, their relative roles, particularly wildlife, remain to be ascertained. As cercarial emergence is a heritable trait shaped by the definitive hosts’ behaviour, three chronobiological trials of cercarial emergence from field-collected snails from two contrasting ecological regions within China were performed, followed by genetic analyses of the parasites. Two distinct modes were identified, with late afternoon emergence mainly found in the hill region, compatible with a nocturnal rodent reservoir, and early emergence within the marshland consistent with a diurnal cattle reservoir. Furthermore, genetic analyses pointed to a clear separation between cercariae with different biological traits. The phenotypic and genotypic differentiation of the parasites identified here between and within two regions may indicate a strain complex. Such parasite diversity could, in turn, provide an explanation for the different infection scenarios observed between the two regions, and hence have important applied implications in terms of targeted control of key reservoirs.