The evolution of strong reproductive isolation between sympatric intertidal snails

Philos Trans R Soc Lond B Biol Sci. 2020 Aug 31;375(1806):20190545. doi: 10.1098/rstb.2019.0545. Epub 2020 Jul 13.

Abstract

The evolution of strong reproductive isolation (RI) is fundamental to the origins and maintenance of biological diversity, especially in situations where geographical distributions of taxa broadly overlap. But what is the history behind strong barriers currently acting in sympatry? Using whole-genome sequencing and single nucleotide polymorphism genotyping, we inferred (i) the evolutionary relationships, (ii) the strength of RI, and (iii) the demographic history of divergence between two broadly sympatric taxa of intertidal snail. Despite being cryptic, based on external morphology, Littorina arcana and Littorina saxatilis differ in their mode of female reproduction (egg-laying versus brooding), which may generate a strong post-zygotic barrier. We show that egg-laying and brooding snails are closely related, but genetically distinct. Genotyping of 3092 snails from three locations failed to recover any recent hybrid or backcrossed individuals, confirming that RI is strong. There was, however, evidence for a very low level of asymmetrical introgression, suggesting that isolation remains incomplete. The presence of strong, asymmetrical RI was further supported by demographic analysis of these populations. Although the taxa are currently broadly sympatric, demographic modelling suggests that they initially diverged during a short period of geographical separation involving very low gene flow. Our study suggests that some geographical separation may kick-start the evolution of strong RI, facilitating subsequent coexistence of taxa in sympatry. The strength of RI needed to achieve sympatry and the subsequent effect of sympatry on RI remain open questions. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

Keywords: Littorina arcana; Littorina saxatilis; demographic inference; reproductive mode; speciation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • England
  • France
  • Gene Flow*
  • Genetic Speciation*
  • Reproductive Isolation*
  • Snails / genetics
  • Snails / physiology*
  • Sympatry*
  • Wales

Associated data

  • figshare/10.6084/m9.figshare.c.5018468