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Morphological and genomic characterisation of the Schistosoma hybrid infecting humans in Europe reveals admixture between Schistosoma haematobium and Schistosoma bovis

Abstract : Schistosomes cause schistosomiasis, the world’s second most important parasitic disease after malaria in terms of public health and social-economic impacts. A peculiar feature of these dioecious parasites is their ability to produce viable and fertile hybrid offspring. Originally only present in the tropics, schistosomiasis is now also endemic in southern Europe. Based on the analysis of two genetic markers the European schistosomes had previously been identified as hybrids between the livestock- and the human-infective species Schistosoma bovis and Schistosoma haematobium, respectively. Here, using PacBio long-read sequencing technology we performed genome assembly improvement and annotation of S. bovis, one of the parental species for which no satisfactory genome assembly was available. We then describe the whole genome introgression levels of the hybrid schistosomes, their morphometric parameters (eggs and adult worms) and their compatibility with two European snail strains used as vectors (Bulinus truncatus and Planorbarius metidjensis). Schistosome-snail compatibility is a key parameter for the parasites life cycle progression, and thus the capability of the parasite to establish in a given area. Our results show that this Schistosoma hybrid is strongly introgressed genetically, composed of 77% S. haematobium and 23% S. bovis origin. This genomic admixture suggests an ancient hybridization event and subsequent backcrosses with the human-specific species, S. haematobium, before its introduction in Corsica. We also show that egg morphology (commonly used as a species diagnostic) does not allow for accurate hybrid identification while genetic tests do. Author summary In 2013, schistosomiasis reached Southern Europe. Since then, endemic infections were recurrently identified clearly indicating that the parasite has settled and established locally. Using two molecular markers, we had previously demonstrated that the parasite was a hybrid between Schistosoma haematobium and Schistosoma bovis, two species known to infect humans and livestock, respectively. Nevertheless, this method has very low resolution and is not informative for determining the origins and the mechanisms of hybridization events, e.g. if the hybrid had been recently generated in Corsica or long before it's introduction. The genome-wide sequencing approach, used in this study, allowed us to reveal genomic admixture suggesting that these hybrids are the result of ancient crossing events between S. haematobium and S. bovis, with subsequent backcrossing with S. haematobium. This introgression has prevented compatibility with P. metidjensis snail vectors, which are specific to S. bovis. Additionally, whether in Africa or in Europe, a clear discrepancy exists between the egg shape usually used for species identification and the genomic composition of schistosomes. Therefore, egg shape cannot be used as a good indicator for hybrid detection. Knowing the phenotypic traits and the genetic features of such hybrids may have important implications in terms of diagnostics and disease management either through vector control strategies or treatment of patients.
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Submitted on : Monday, January 3, 2022 - 4:03:22 PM
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Distributed under a Creative Commons Attribution 4.0 International License

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Julien Kincaid-Smith, Alan Tracey, Ronaldo de Carvalho Augusto, Ingo Bulla, Nancy Holroyd, et al.. Morphological and genomic characterisation of the Schistosoma hybrid infecting humans in Europe reveals admixture between Schistosoma haematobium and Schistosoma bovis. PLoS Neglected Tropical Diseases, Public Library of Science, 2021, 15 (12), pp.e0010062. ⟨10.1371/journal.pntd.0010062⟩. ⟨hal-03508340⟩

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