Sympatric and allopatric evolutionary contexts shape differential immune response in Biomphalaria / Schistosoma interaction

Abstract

Selective pressures between hosts and their parasites can result in reciprocal evolution or adaptation of specific life history traits. Local adaptation of resident hosts and parasites should lead to host-parasite systems performing better in sympatry when compared to allopatry. Between-population variations in parasite infectivity/virulence and host defence/resistance, referred to as compatibility phenotype, were often the proxy used to analyse sympatric or allopatric adaptation. Nevertheless, some reported cases exist where allopatric host-parasite systems demonstrate compatibility phenotypes similar or greater than the one observed in sympatry. In these cases, the role of local adaptation is worth considering. Here, we study the interaction between Schistosoma and its vector snail Biomphalaria in which such a discrepancy in local versus foreign compatibility phenotype has been observed. Herein, we developed an integrative approach to investigate sympatric and allopatric interaction processes and link the underlying molecular mechanisms to the resulting phenotypes. Using comparative \"omics\" approaches joined to analysis of life history traits (immune cellular response, mortality, prevalence and compatibility) we tried to bridge the gap of knowledge that exists for connecting local adaptation observations to molecular phenotypes in Schistosoma/Biomphalaria interactions.\n\nWe found that despite displaying similar prevalence phenotypes, parasite infection triggered an immune suppression in snails living in sympatry, while it activated an immune response for those living in allopatry. Dual-comparative molecular analyses revealed that parasite infection causes immune suppression in sympatry. miRNAs were used to hijack the hosts immune response, allowing sympatric parasites to initiate their developmental program earlier and more efficiently.\n\nWe show that despite having similar prevalence phenotypes, sympatric and allopatric snail-Schistosoma interactions displayed a strongly different immunobiological molecular dialogue. The ability of allopatric pathogens to adapt rapidly and efficiently to new hosts could have critical consequences on disease emergence and risk of schistosomiasis outbreaks. These observations would have important consequences in term of schistosomiasis disease control.