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

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 increase parasite infectivity/virulence (higher compatibility) when infecting hosts from the same location (in sympatry) than from a foreign location (in allopatry). Analysis of geographic variations in compatibility phenotypes is the most common proxy used to infer local adaptation. However, in some cases, allopatric host-parasite systems demonstrate similar or greater compatibility than in sympatry. In such cases, the potential for local adaptation remains unclear. Here, we study the interaction between Schistosoma and its vector snail Biomphalaria in which such discrepancy in local versus foreign compatibility phenotype has been reported. Herein, we aim at bridging this gap of knowledge by comparing life history traits (immune cellular response, host mortality, and parasite growth) and molecular responses in highly compatible sympatric and allopatric Schistosoma/Biomphalaria interactions originating from different geographic localities (Brazil, Venezuela and Burundi). We found that despite displaying similar prevalence phenotypes, sympatric schistosomes triggered a rapid immune suppression (dual-RNAseq analyses) in the snails within 24h post infection, whereas infection by allopatric schistosomes (regardless of the species) was associated with immune cell proliferation and triggered a non-specific generalized immune response after 96h. We observed that, sympatric schistosomes grow more rapidly. Finally, we identify miRNAs differentially expressed by Schistosoma mansoni that target host immune genes and could be responsible for hijacking the host immune response during the sympatric interaction. We show that despite having similar prevalence phenotypes, sympatric and allopatric snail-Schistosoma interactions displayed strong differences in their immunobiological molecular dialogue. Understanding the mechanisms allowing parasites to adapt rapidly and efficiently to new hosts is critical to control disease emergence and risks of Schistosomiasis outbreaks.Author summarySchistosomiasis, the second most widespread human parasitic disease after malaria, is caused by helminth parasites of the genus Schistosoma. More than 200 million people in 74 countries suffer from the pathological, and societal consequences of this disease. To complete its life cycle, the parasite requires an intermediate host, a freshwater snail of the genus Biomphalaria for its transmission. Given the limited options for treating Schistosoma mansoni infections in humans, much research has focused on developing methods to control transmission by its intermediate snail host. Biomphalaria glabrata. Comparative studies have shown that infection of the snail triggers complex cellular and humoral immune responses resulting in significant variations in parasite infectivity and snail susceptibility, known as the so-called polymorphism of compatibility. However, studies have mostly focused on characterizing the immunobiological mechanisms in sympatric interactions. Herein we used a combination of molecular and phenotypic approaches to compare the effect of infection in various sympatric and allopatric evolutionary contexts, allowing us to better understand the mechanisms of host-parasite local adaptation. Learning more about the immunobiological interactions between B. glabrata and S. mansoni could have important socioeconomic and public health impacts by changing the way we attempt to eradicate parasitic diseases and prevent or control schistosomiasis in the field.