Secondary contacts between European white oaks reveal genes underlying reproductive isolation. BAN

Oaks are dominant forest tree species widely distributed across the Northern hemisphere, where they constitute natural resources of economical, ecological, social and historical value. Hybridization and adaptive introgression has long been advocated as a major evolutionary driver of their ecological success. Yet, a key question of their diversification in the context of interspecific gene flow is the maintenance of species barriers. Here, we developed a demographically-explicit genome scan approach combining Approximate Bayesian Computation and backward simulations to scan genomes of four European white oak species for reproductive barriers. We first confirmed earlier findings highlighting interspecific contacts occurring after the last glacial maximum. We then took advantage of the huge genetic variation observed between these four species (31 106 SNPs) to identify genomic regions mostly enriched in SNPs deviating from demographic expectations under recent secondary contacts. Detected outlier-enriched regions were restricted in size, widely distributed over all chromosomes. Our scan detected 215 regions containing 227 oak genes. Literature-based functional annotation of the underlying genes highlighted important functions driving reproductive isolation between the four species. These included genes involved in tolerance to biotic and abiotic constraints, and in intrinsic mating barriers. The functions of the annotated genes fit well with the ecological preferences of the four species. Hence these genes may be considered as candidates to investigate species responses to past and ongoing environmental changes.

橡树（oak）是广泛分布于北半球的优势森林树种，亦是兼具经济、生态、社会与历史多重价值的重要自然资源。杂交与适应性渐渗（adaptive introgression）长期以来被认为是推动其生态成功的主要进化驱动力。然而，在种间基因流的背景下，其物种分化的核心问题之一是物种屏障的维持。本研究开发了一种结合近似贝叶斯计算（Approximate Bayesian Computation）与回溯模拟的显式种群历史基因组扫描方法，用于对4种欧洲白橡树的基因组开展生殖屏障筛查。研究首先验证了此前的研究结论，即末次盛冰期后发生了种间基因交流。随后，研究利用4个物种间观测到的海量遗传变异（共计31106个单核苷酸多态性（Single Nucleotide Polymorphisms，SNPs）），筛选出在近期次生接触场景下显著偏离种群历史预期的单核苷酸多态性富集基因组区域。检测到的异常位点富集基因组区域尺寸较小，且广泛分布于所有染色体上。本次基因组扫描共检测到215个相关区域，涵盖227个橡树基因。通过文献调研对这些候选基因开展功能注释后发现，多个关键功能与4个物种间的生殖隔离形成密切相关，包括参与生物与非生物胁迫耐受的基因，以及调控内在交配障碍的相关基因。注释基因的功能与这4个白橡树物种的生态偏好高度契合。因此，这些基因可作为研究物种对过去及当前环境变化响应的候选靶标。