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'.

强生殖隔离 (RI) 的进化是生物多样性起源和维持的基础，尤其是在分类群地理分布广泛重叠的情况下。但是，目前表现出同情的强大障碍背后的历史是什么？使用全基因组测序和单核苷酸多态性基因分型，我们推断出 (i) 进化关系，(ii) RI 的强度，以及 (iii) 潮间带蜗牛的两个广泛同域分类群之间差异的人口统计历史。尽管很神秘，但基于外部形态，Littorina arcana和Littorina saxatilis它们的雌性繁殖方式（产卵与育雏）不同，这可能会产生强大的合子后屏障。我们表明产卵和育雏蜗牛密切相关，但在遗传上是不同的。来自三个地点的 3092 只蜗牛的基因分型未能恢复任何最近的杂交或回交个体，证实 RI 很强。然而，有证据表明不对称基因渗入的水平非常低，这表明隔离仍然不完整。对这些人群的人口统计分析进一步支持了强、不对称 RI 的存在。尽管这些分类群目前大致是同域的，但人口模型表明，它们最初是在涉及极低基因流的短期地理分离期间发生分歧的。我们的研究表明，一些地理上的分离可能会启动强 RI 的进化，促进随后分类群的共存。实现同情所需的 RI 强度以及同情对 RI 的后续影响仍然是悬而未决的问题。

本文是主题问题“走向物种形成的完成：超越第一道障碍的生殖隔离的进化”的一部分。