Analysis of genomic divergence landscape in recurrently hybridising Chironomus sister taxa suggests stable steady-state between mutual gene-flow and isolation

By virtue of steadily accumulating evidence, divergence with gene-flow is now a recognised mode of speciation. Current models suggest that diverging lineages inevitably become completely reproductively and genomically isolated. We tested this hypothesis by analysing the divergence landscape between two recurrently hybridising sister species of non-biting midges, Chironomus riparius and C. piger. Using a principal component based method, we estimated that 28.44% of the genome were mutually isolated, containing 49.4% of the annotated genes. These genes were enriched for processes and structure requiring close molecular collaboration. Divergence landscape was fragmented, distributed throughout the genome and isolation regions on average 30 kb small. Evidence for recent divergent selection processes was scarce, while traces of purifying selection were abundant in the isolated regions. Comparing the observed distribution of divergence time estimates with coalescence simulations implies that most of divergence happened during a short time span about 4.5 mio generations ago. We suggest that the observed steady-state equilibrium between mutual gene-flow and isolation is due to seasonal hybridisation, high migration rates and high Ne favouring rapid purification. Our findings thus extent the speciation with gene flow paradigm with evidence for long diverged “good” sister species that nevertheless share large parts of their genomes.

随着相关研究证据的持续积累，基因流存在下的物种分化（divergence with gene-flow）现已成为公认的物种形成模式。现有模型认为，正在分化的谱系最终会完全实现生殖隔离与基因组隔离。本研究以两种反复发生杂交的摇蚊姊妹物种——Chironomus riparius和C. piger——的分化景观为研究对象，对上述假说进行了验证。本研究采用基于主成分分析的方法，估算得到28.44%的基因组区域存在相互隔离，其中包含了49.4%的已注释基因。这些基因富集于需要紧密分子协作的生物学过程及结构形成相关功能。分化景观呈现碎片化特征，分布于整个基因组中，且隔离区域的平均长度仅为30千碱基对（kb）。未检测到近期歧化选择的显著信号，但隔离区域中存在大量纯化选择的痕迹。将实测的分化时间估算分布与溯祖模拟（coalescence simulations）结果进行对比后发现，绝大多数基因组分化发生在约450万代前的短暂时期内。本研究认为，观测到的基因流与基因组隔离间的稳态平衡，源于季节性杂交、高迁移率以及高有效种群规模（Ne）所带来的快速纯化效应。本研究结果拓展了基因流存在下的物种形成范式，提供了分化已久的‘真正’姊妹物种仍共享大部分基因组序列的实证依据。