Whole-genome sequencing data of Formica aquilonia and F. polyctena individuals. Formica speciation history

The application of demographic history modelling and inference to the study of divergence between species has become a cornerstone of speciation genomics. Speciation histories are usually reconstructed by analysing single populations from each species, assuming that the inferred population history represents the actual speciation history. However, this assumption may not be met when species diverge with gene flow, e.g., when secondary contact may be confined to specific geographic regions. Here, we tested whether divergence histories inferred from heterospecific populations may vary depending on their geographic locations, using the two wood ant species Formica polyctena and F. aquilonia. We performed whole-genome resequencing of 20 individuals sampled in multiple locations across the European ranges of both species. Then, we reconstructed the histories of distinct heterospecific population pairs using a coalescent-based approach. Our analyses always supported a scenario of divergence with gene flow, suggesting that divergence started in the Pleistocene (ca. 500 kya) and occurred with continuous asymmetrical gene flow from F. aquilonia to F. polyctena until a recent time, when migration became negligible (2-19 kya). However, we found support for contemporary gene flow in a sympatric pair from Finland, where the species hybridise, but no signature of recent bidirectional gene flow elsewhere. Overall, our results suggest that divergence histories reconstructed from a few individuals may be applicable at the species level. Nonetheless, the geographical context of populations chosen to represent their species should be taken into account, as it may affect estimates of migration rates between species when gene flow is spatially heterogeneous.

种群历史建模与推断在物种间分化研究中的应用，已成为物种形成基因组学（speciation genomics）的核心研究支柱。以往研究通常通过分析每个物种的单个种群来重建物种形成历史，并默认所推断的种群历史即可代表真实的物种形成历程。然而，当物种间存在基因流时，这一假设或难以成立——例如当二次接触仅局限于特定地理区域时。本研究以两种木蚁——红褐林蚁（Formica polyctena）与黑褐林蚁（F. aquilonia）为研究对象，旨在检验基于异种种群推断的分化历史是否会因采样地理位置的差异而有所不同。我们对采自两个物种欧洲自然分布范围内多个地点的20个个体开展了全基因组重测序（whole-genome resequencing）。随后，采用基于溯祖（coalescent-based）的分析方法，对多组不同的异种种群对的演化历史进行了重建。所有分析结果均支持存在基因流的分化场景，表明两个物种的分化始于更新世（约50万年前），且其间持续存在从黑褐林蚁向红褐林蚁的不对称基因流，直至约2至1.9万年前，迁移事件才变得可忽略不计。不过，我们在芬兰的一个同域分布种群对中发现了当代基因流的证据——此处两个物种存在自然杂交，但在其余采样区域均未检测到近期双向基因流的信号。总体而言，本研究结果表明，基于少量个体重建的分化历史或可推广至物种水平。但在选取代表物种的种群样本时，仍需充分考虑其地理背景：当基因流存在空间异质性时，该背景可能会对物种间迁移速率的估计产生影响。