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

Type Article
Date 2021-05
Language English
Author(s) Kincaid-Smith Julien1, Mathieu-Bégné EglantineORCID2, Chaparro CristianORCID2, Reguera-Gomez MartaORCID3, Mulero StephenORCID2, Allienne Jean-FrancoisORCID2, Toulza EveORCID2, Boissier JérômeORCID2, Lamberton Poppy H. L.2
Affiliation(s) 1 : Univ. Montpellier, CNRS, IFREMER, UPVD, IHPE, Perpignan, France
2 : Centre for Emerging, Endemic and Exotic Diseases (CEEED), Department of Pathobiology and Population Sciences (PPS), Royal Veterinary College, University of London, Hawkshead Campus, Herts, United Kingdom
3 : Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Burjassot, Valencia, Spain
Source Plos Neglected Tropical Diseases (1935-2735) (Public Library of Science (PLoS)), 2021-05 , Vol. 15 , N. 5 , P. e0009363 (24p.)
DOI 10.1371/journal.pntd.0009363
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.

Full Text
File Pages Size Access
Publisher's official version 24 2 MB Open access
S1 Table. Metrics of the RNA-sequencing reads processing 11 KB Open access
S1 File. Transcriptome analysis related information: Sheet A in S1 File: Table showing the full annotation of the reference transcriptome representative of S. haematobium and S. bovis assembled ... 10 MB Open access
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How to cite 

Kincaid-Smith Julien, Mathieu-Bégné Eglantine, Chaparro Cristian, Reguera-Gomez Marta, Mulero Stephen, Allienne Jean-Francois, Toulza Eve, Boissier Jérôme, Lamberton Poppy H. L. (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), e0009363 (24p.). Publisher's official version : https://doi.org/10.1371/journal.pntd.0009363 , Open Access version : https://archimer.ifremer.fr/doc/00693/80481/