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

Julien Kincaid-Smith,Cristian Chaparro,Jean-Francois Allienne,Marta Reguera-Gomez,Eve Toulza,Stephen Mulero,Jérôme Boissier,Eglantine Mathieu-Bégné

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.

Highlights

A subset of obstacles evolved in the course of speciation in order to limit gene flow via hybridization and maintain species boundaries
We addressed the question of reproductive isolation mechanisms in parasitic species by conducting an integrative experimental study on two schistosome species (Schistosoma haematobium and S. bovis) that parasitize human and cattle, respectively
We showed that rather than having a homo-specific mate choice, S. haematobium and S. bovis mate randomly

Summary

Introduction

A subset of obstacles evolved in the course of speciation in order to limit gene flow via hybridization and maintain species boundaries. These obstacles are traditionally classified as pre- and post-zygotic barriers ( 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]. When the first barrier is crossed, post-zygotic isolation mechanisms can arise to prevent gene flow. Reproductive isolation is often the result of an accumulation and interaction of multiple pre- and post-zygotic mechanisms restricting most gene flow [3]. It is generally recognized that pre-zygotic isolation barriers are enhanced in sympatric species [4], and are the most effective because they act early to prevent the production of hybrid progeny

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