Hybridization is a fascinating evolutionary phenomenon that raises the question of how species maintain their integrity. Inter-species hybridization occurs between certain Schistosoma species that can cause important public health and veterinary issues. In particular hybrids between Schistosoma haematobium and S. bovis associated with humans and animals respectively are frequently identified in Africa. Recent genomic evidence indicates that some S. haematobium populations show signatures of genomic introgression from S. bovis. Here, we conducted a genomic comparative study and investigated the genomic relationships between S. haematobium, S. bovis and their hybrids using 19 isolates originating from a wide geographical range over Africa, including samples initially classified as S. haematobium (n = 11), S. bovis (n = 6) and S. haematobium x S. bovis hybrids (n = 2). Based on a whole genomic sequencing approach, we developed 56,181 SNPs that allowed a clear differentiation of S. bovis isolates from a genomic cluster including all S. haematobium isolates and a natural S. haematobium-bovis hybrid. All the isolates from the S. haematobium cluster except the isolate from Madagascar harbored signatures of genomic introgression from S. bovis. Isolates from Corsica, Mali and Egypt harbored the S. bovis-like Invadolysin gene, an introgressed tract that has been previously detected in some introgressed S. haematobium populations from Niger. Together our results highlight the fact that introgression from S. bovis is widespread across S. haematobium and that the observed introgression is unidirectional.

Species usually develop reproductive isolation mechanisms allowing them to avoid interbreeding. These preventive barriers can act before reproduction, “pre-zygotic barriers”, or after reproduction, “post-zygotic barriers”. Pre-zygotic barriers prevent unfavourable mating, while post-zygotic barriers determine the viability and selective success of the hybrid offspring. Hybridization in parasites and the underlying reproductive isolation mechanisms maintaining their genetic integrity have been overlooked. Using an integrated approach this work aims to quantify the relative importance of pre-zygotic barriers in Schistosoma haematobium x S. bovis crosses. These two co-endemic species cause schistosomiasis, one of the major debilitating parasitic diseases worldwide, and can hybridize naturally. Using mate choice experiments we first tested if a specific mate recognition system exists between both species. Second, using RNA-sequencing we analysed differential gene expression between homo- and hetero-specific pairing in male and female adult parasites. We show that homo- and hetero-specific pairing occurs randomly between these two species, and few genes in both sexes are affected by hetero-specific pairing. This suggests that i) mate choice is not a reproductive isolating factor, and that ii) no pre-zygotic barrier except spatial isolation “by the final vertebrate host” seems to limit interbreeding between these two species. Interestingly, among the few genes affected by the pairing status of the worms, some can be related to pathways affected during male and female interactions and may also present interesting candidates for species isolation mechanisms and hybridization in schistosome parasites.

Understanding the drivers of species distribution is necessary in order to properly predict the future geographical ranges of colonizing species. Yet this task is challenging for species involved in intimate interactions, such as parasites, since their distribution is likely shaped by a complex interplay between environmental‐related and host‐related factors. Here we developed an original approach combining species distribution models (SDMs) and population genomics to test whether the local environmental conditions or the host genomic background most likely limits the colonization of an emerging freshwater fish ectoparasite, Tracheliastes polycolpus . We hypothesized that the absence of T. polycolpus in some areas may be due to an unsuitable environment in these areas (the ‘environmental suitability hypothesis') and/or to the presence of resistant hosts in these areas (the ‘genomic background hypothesis'). Using a SDM set at the French spatial extent, we first found that the environmental conditions of an uninfected area were as suitable for the parasite as those of infected areas. Then, using single nucleotide polymorphisms (SNPs) data at the host genome scale, we demonstrated that there was a strong association between the spatial occurrence of parasites and the host genomic background. In particular, the area in which the parasite was absent sustained a unique host population from a genomic standpoint, and ninety SNPs were significantly associated to the infection status (parasitized versus unparasitized) of individual hosts. We concluded that the spatial distribution of T. polycolpus (and its colonization potential) was more likely limited by intrinsic host characteristics associated to parasite resistance, rather than to the local environmental conditions. This study illustrates the usefulness of combining modeling and genomic approaches to reveal the determinants of species distribution and to improve predictions about their future ranges.

Recent studies have highlighted associations between diseases and host microbiota. It remains extremely challenging – especially under natural conditions – to clarify whether host microbiota promote future infections, or whether changes in host microbiota result from infections. Nonetheless, deciphering between these two processes is essential for highlighting the role of microbes in disease progression. We longitudinally surveyed, in the wild, the microbiota of individual fish hosts (Leuciscus burdigalensis) both before and after infection by a crustacean ectoparasite (Tracheliastes polycolpus). We found a striking association between parasite infection and the host microbiota composition restricted to the fins the parasite anchored. We clearly demonstrated that infections by the parasite induced a shift in (and did not result from) the host fin microbiota. Furthermore during infection, the microbiota of infected fins got similar to the microbiota of the adult stage, and the free‐living infective stage of the parasite with a predominance of the Burkholderiaceae bacteria family. This suggests that some Burkholderiaceae bacteria are involved in a coinfection process and possibly facilitate T. polycolpus infection. In this study, we reveal novel mechanistic insights for understanding the role of the microbiota in host–parasite interactions, which has implications for predicting the progression of diseases in natural host populations.

When two species hybridize, the two parental genomes are brought together and some alleles might interact for the first time. To date, the extent of the transcriptomic changes in first hybrid generations, along with their functional outcome constitute an important knowledge gap, especially in parasite species. Here we explored the molecular and functional outcomes of hybridization in first-generation hybrids between the blood fluke parasites Schistosoma haematobium and S. bovis. Through a transcriptomic approach, we measured gene expression in both parental species and hybrids. We described and quantified expression profiles encountered in hybrids along with the main biological processes impacted. Up to 7,100 genes fell into a particular hybrid expression profile (intermediate between the parental expression levels, over-expressed, under-expressed, or expressed like one of the parental lines). Most of these genes were different depending on the direction of the parental cross (S. bovis mother and S. haematobium father or the reverse) and depending on the sex. For a given sex and cross direction, the vast majority of genes were hence unassigned to a hybrid expression profile: either they were differentially expressed genes but not typical of any hybrid expression profiles or they were not differentially expressed neither between hybrids and parental lines nor between parental lines. The most prevalent profile of gene expression in hybrids was the intermediate one (24% of investigated genes). These results suggest that transcriptomic compatibility between S. haematobium and S. bovis remains quite high. We also found support for an over-dominance model (over- and under-expressed genes in hybrids compared to parental lines) potentially associated with heterosis. In females in particular, processes such as reproductive processes, metabolism and cell interactions as well as signaling pathways were indeed affected. Our study hence provides new insight on the biology of Schistosoma hybrids with evidences supporting compatibility and heterosis.