No pre-zygotic isolation mechanisms between Schistosoma haematobium and Schistosoma bovis parasites: From mating interactions to differential gene expression

Kincaid-Smith, J; Mathieu-Begne, E; Chaparro, C; Reguera-Gomez, M; Mulero, S; Allienne, JF; Toulza, E; Boissier, J

Abstract

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. Author summary Understanding how species maintain their genetic integrity is a central question in evolutionary biology. While isolation mechanisms are well documented in free-living organisms, it is currently not the case for parasite species. Yet, occurrence of parasite hybrids is a critical global health concern since these hybrids are expected to be more harmful than parental species. We addressed the question of reproductive isolation mechanisms in parasitic species by conducting an integrative experimental study (from mate choice to gene expression) on two schistosome species (Schistosoma haematobium and S. bovis) that parasitize human and cattle, respectively. Importantly, their hybrid progeny has been involved in recent outbreaks, including outbreaks outside of endemic areas. We showed that rather than having a homo-specific mate choice, S. haematobium and S. bovis mate randomly. Also, male and female worms only express a few genes differentially when involved in a hetero-specific pair compared to a homo-specific pair. We consequently suggest that these two schistosome species lack strong reproduction isolation mechanisms, except those imposed by specificity to the final host species. Our results raise the concern that in the absence of post-zygotic barriers in sympatric zones hybridization might be more common than previously thought if these two species are able to encounter each other.

Citation

Kincaid-Smith, J., Mathieu-Begne, E., Chaparro, C., Reguera-Gomez, M., Mulero, S., Allienne, J., …Boissier, J. (2021). No pre-zygotic isolation mechanisms between Schistosoma haematobium and Schistosoma bovis parasites: From mating interactions to differential gene expression. PLoS Neglected Tropical Diseases, 15(5), https://doi.org/10.1371/journal.pntd.0009363

• Journal Article Type: Article
• Acceptance Date: May 3, 2021
• Publication Date: 2021
• Deposit Date: Dec 22, 2021
• Publicly Available Date: Dec 22, 2021
• Print ISSN: 1935-2727
• Publisher: Public Library of Science
• Peer Reviewed: Peer Reviewed
• Volume: 15
• Issue: 5
• DOI: https://doi.org/10.1371/journal.pntd.0009363
• Keywords: BIOMPHALARIA-GLABRATA; REPRODUCTIVE-ORGANS; MIXED INFECTIONS; ONE HEALTH; MANSONI; HYBRIDIZATION; INTERCALATUM; BEHAVIOR; SNAIL; INTROGRESSION
• Public URL: https://rvc-repository.worktribe.com/output/1553747