Epigenetic origin of adaptive phenotypic variants in the blood-fluke Schistosoma mansoni

Abstract

Adaptive evolution is impossible without the generation of phenotypic variants. The origin of variation has been a central topic in evolutionary biology. It is now commonly accepted that genetic variation is the only cause of phenotypic variants. The term “mutant” is even often used interchangeable to designate a genetic or a phenotypic variation. However, epigenetic information is emerging as a complementary source of heritable phenotypic variation. It is currently not clear what the relative importance of genetics and epigenetics in generating this variation is. We used a host-parasite system to address this question. The human blood fluke Schistosoma mansoni can adapt rapidly to new intermediate snail hosts. The interaction between parasite and mollusk is characterized by a compatibility polymorphism. The principal molecular marker for compatibility (infection success) is the expression pattern of polymorphic mucins (SmPoMuc). We show here that chromatin structure changes at the SmPoMuc promoters are the principal cause for SmPoMuc transcription polymorphism leading to phenotypic novelty and increase in infection success i.e. fitness. We establish that epigenetic changes can be the major if not only cause of adaptive phenotypic variants in Schistosoma mansoni, suggesting that epimutations can provide material for adaptive evolution in the absence of genetic variation.