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No Pre-Zygotic Isolation Mechanisms Between Schistosoma No pre-zygotic isolation mechanisms between Schistosoma haematobium and Schistosoma bovis parasites: From mating interactions to differential gene expression Julien Kincaid-Smith, Eglantine Mathieu-Bégné, Cristian Chaparro, Marta Reguera-Gomez, Stephen Mulero, Jean-Francois Allienne, Eve Toulza, Jérôme Boissier To cite this version: Julien Kincaid-Smith, Eglantine Mathieu-Bégné, Cristian Chaparro, Marta Reguera-Gomez, Stephen Mulero, et al.. No pre-zygotic isolation mechanisms between Schistosoma haematobium and Schisto- soma bovis parasites: From mating interactions to differential gene expression. PLoS Neglected Trop- ical Diseases, Public Library of Science, 2021, 15 (5), pp.e0009363. 10.1371/journal.pntd.0009363. hal-03255515 HAL Id: hal-03255515 https://hal.archives-ouvertes.fr/hal-03255515 Submitted on 9 Jun 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. RESEARCH ARTICLE No pre-zygotic isolation mechanisms between Schistosoma haematobium and Schistosoma bovis parasites: From mating interactions to differential gene expression 1,2³ 1³ 1 Julien Kincaid-Smith , Eglantine Mathieu-BeÂgne ID *, Cristian ChaparroID , 3 1 1 1 Marta Reguera-GomezID , Stephen MuleroID , Jean-Francois AllienneID , Eve ToulzaID , 1 JeÂroà me BoissierID * 1 Univ. Montpellier, CNRS, IFREMER, UPVD, IHPE, Perpignan, France, 2 Centre for Emerging, Endemic a1111111111 and Exotic Diseases (CEEED), Department of Pathobiology and Population Sciences (PPS), Royal a1111111111 Veterinary College, University of London, Hawkshead Campus, Herts, United Kingdom, 3 Departamento de a1111111111 ParasitologõÂa, Facultad de Farmacia, Universidad de Valencia, Burjassot, Valencia, Spain a1111111111 ³ These authors share first authorship on this work. a1111111111 * [email protected] (EM-B); [email protected] (JB) Abstract OPEN ACCESS Species usually develop reproductive isolation mechanisms allowing them to avoid inter- Citation: Kincaid-Smith J, Mathieu-BeÂgne E, breeding. These preventive barriers can act before reproduction, ªpre-zygotic barriersº, or Chaparro C, Reguera-Gomez M, Mulero S, Allienne J-F, et al. (2021) No pre-zygotic isolation after reproduction, ªpost-zygotic barriersº. Pre-zygotic barriers prevent unfavourable mating, mechanisms between Schistosoma haematobium while post-zygotic barriers determine the viability and selective success of the hybrid off- and Schistosoma bovis parasites: From mating spring. Hybridization in parasites and the underlying reproductive isolation mechanisms interactions to differential gene expression. PLoS maintaining their genetic integrity have been overlooked. Using an integrated approach this Negl Trop Dis 15(5): e0009363. https://doi.org/ 10.1371/journal.pntd.0009363 work aims to quantify the relative importance of pre-zygotic barriers in Schistosoma haema- tobium x S. bovis crosses. These two co-endemic species cause schistosomiasis, one of Editor: Poppy H. L. Lamberton, University of Glasgow School of Life Sciences, UNITED the major debilitating parasitic diseases worldwide, and can hybridize naturally. Using mate KINGDOM choice experiments we first tested if a specific mate recognition system exists between both Received: September 4, 2020 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- Accepted: April 6, 2021 and hetero-specific pairing occurs randomly between these two species, and few genes in Published: May 4, 2021 both sexes are affected by hetero-specific pairing. This suggests that i) mate choice is not a Peer Review History: PLOS recognizes the reproductive isolating factor, and that ii) no pre-zygotic barrier except spatial isolation ªby benefits of transparency in the peer review the final vertebrate hostº seems to limit interbreeding between these two species. Interest- process; therefore, we enable the publication of all of the content of peer review and author ingly, among the few genes affected by the pairing status of the worms, some can be related responses alongside final, published articles. The to pathways affected during male and female interactions and may also present interesting editorial history of this article is available here: candidates for species isolation mechanisms and hybridization in schistosome parasites. https://doi.org/10.1371/journal.pntd.0009363 Copyright: © 2021 Kincaid-Smith et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0009363 May 4, 2021 1 / 24 PLOS NEGLECTED TROPICAL DISEASES No pre-zygotic barriers between schistosome species Data Availability Statement: The authors confirm that all data underlying the findings are fully Author summary available without restriction. Raw sequences used in this study have been submitted to the Sequence Understanding how species maintain their genetic integrity is a central question in evolu- Read Archive under the BioProject PRJNA491632, tionary biology. While isolation mechanisms are well documented in free-living organ- the transcriptome assembly have been submitted isms, it is currently not the case for parasite species. Yet, occurrence of parasite hybrids is on the Figshare repository (https://doi.org/10.6084/ a critical global health concern since these hybrids are expected to be more harmful than m9.figshare.12581156). parental species. We addressed the question of reproductive isolation mechanisms in par- Funding: This work has been funded by the French asitic species by conducting an integrative experimental study (from mate choice to gene Research National Agency (project HySWARM, expression) on two schistosome species (Schistosoma haematobium and S. bovis) that par- grant no. ANR-18-CE35-0001). SM was supported asitize human and cattle, respectively. Importantly, their hybrid progeny has been by the Occitania region (project MOLRISK, award no. NREST 2019/1/059), the European ªFonds involved in recent outbreaks, including outbreaks outside of endemic areas. We showed EuropeÂen de DeÂveloppement ReÂgionalº (FEDER) that rather than having a homo-specific mate choice, S. haematobium and S. bovis mate and MRG by the Fellowship of "Estancias breves" randomly. Also, male and female worms only express a few genes differentially when (linked to the Programa de Ayudas de Formacion involved in a hetero-specific pair compared to a homo-specific pair. We consequently sug- de Profesorado Universitario 2015, Ministerio de gest that these two schistosome species lack strong reproduction isolation mechanisms, Ciencia, InnovacioÂn y Universidades, Spain, https:// www.educacionyfp.gob.es/servicios-al-ciudadano/ except those imposed by specificity to the final host species. Our results raise the concern catalogo/general/20/200487/ficha/200487-2017. that in the absence of post-zygotic barriers in sympatric zones hybridization might be html#dc1). The funders had no role in study more common than previously thought if these two species are able to encounter each design, data collection and analysis, decision to other. publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Introduction A subset of obstacles evolved in the course of speciation in order to limit gene flow via hybrid- ization and maintain species boundaries. These obstacles are traditionally classified as pre- and post-zygotic barriers (also known as pre- or post-mating barriers) and can be defined as any mechanism preventing or reducing gene flow between groups of potentially interbreeding individuals [1]. Pre-zygotic barriers include spatial isolation (e.g., two species live in different habitats), behavioural isolation (e.g., individuals can choose to mate with individuals of their own species), temporal isolation (reproduction does not occur at the same time e.g., different seasons), mechanical isolation (sex organs are not compatible) and gametic isolation (sperm and eggs mix but fertilization does not occur). When the first barrier is crossed, post-zygotic isolation mechanisms can arise to prevent gene flow. Post-zygotic barriers include hybrid unviability (hybrids die prematurely), reduced fitness with low fertility (hybrids are less fertile, infertile or non-viable) or hybrid breakdown (a longer process where the hybrid lines are counter-selected compared to their parental forms). The strength and/or the order of each reproductive barrier vary among species. This makes difficult to predict the outcome of inter- species mating, and the evolution of reproductive isolation mechanisms [2]. Moreover, repro- ductive isolation is often the result of an accumulation and interaction of multiple pre- and post-zygotic mechanisms restricting most gene flow [3]. However, it is generally recognized that pre-zygotic isolation barriers
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