Approximate Bayesian computation untangles signatures of contemporary and historical hybridization between two endangered Arabis floodplain species

Contemporary gene flow, when resumed after a period of isolation, can have crucial consequences for endangered species, as it can both increase the supply of adaptive alleles and erode local adaptation. Determining the history of gene flow and thus the importance of contemporary hybridization, however, is notoriously difficult. Here, we focus on two endangered plant species, Arabis nemorensis and A. sagittata, which hybridize naturally in a sympatric population located on the banks of the Rhine. Using reduced genome sequencing, we determined the phylogeography of the two taxa but report only a unique sympatric population. Molecular variation in chloroplast DNA indicated that A. sagittata is the principal receiver of gene flow. Applying classical D-statistics and its derivatives to whole-genome data of 35 accessions, we detect gene flow not only in the sympatric population but also among allopatric populations. Using an Approximate Bayesian computation approach, we identify the model that best describes the history of gene flow between these taxa. This model shows that low levels of gene flow have persisted long after speciation. Around 10 000 years ago, gene flow stopped and a period of complete isolation began. Eventually, a hotspot of contemporary hybridization was formed in the unique sympatric population. Occasional sympatry may have helped protect these lineages from extinction in spite of their extremely low diversity.

当代基因流在经历一段时期的隔离后再度发生时，会对濒危物种产生至关重要的影响：它既可以增加适应性等位基因的供给，也可能削弱本地适应性。然而，厘清基因流的历史并由此明确当代杂交的重要性，向来极具挑战。本研究聚焦两种濒危植物：林生南芥（Arabis nemorensis）和箭叶南芥（A. sagittata），二者在莱茵河沿岸的同域种群中自然杂交。本研究通过简化基因组测序技术，解析了这两个类群的系统地理学格局，但仅报道了一处独特的同域种群。叶绿体DNA的分子变异分析显示，箭叶南芥是此次基因流的主要接收方。我们将经典D统计量（D-statistics）及其衍生方法应用于35份种质的全基因组数据，不仅在同域种群中检测到了基因流，在异域种群间也发现了基因流现象。通过近似贝叶斯计算（Approximate Bayesian computation）方法，我们筛选出了最能描述这两个类群间基因流历史的模型。该模型表明，在物种形成之后，低水平的基因流仍持续了相当长的一段时间。大约一万年前，基因流完全终止，二者进入了彻底隔离的阶段。最终，在这处独特的同域种群中形成了当代杂交热点。尽管这两个类群的遗传多样性极低，但偶尔的同域分布可能帮助它们避免了灭绝。