Data from: Positive selection on sperm ion channels in a brooding brittle star: consequence of life-history traits evolution

Closely related species are key models to investigate mechanisms leading to reproductive isolation and early stages of diversification, also at the genomic level. The brittle star cryptic species complex Ophioderma longicauda encompasses the sympatric broadcast spawning species C3 and the internal brooding species C5. Here we used de novo transcriptome sequencing and assembly in two closely related species displaying contrasting reproductive modes to compare their genetic diversity and to investigate the role of natural selection in reproductive isolation. We reconstructed 20,146 and 22,123 genes for C3 and C5, respectively, and characterized a set of 12,229 orthologs. Genetic diversity was 1.5-2 times higher in C3 compared to C5, confirming that species with low parental investment display higher levels of genetic diversity. Forty-eight genes were the targets of positive diversifying selection during the evolution of the two species. Notably, two genes (NHE and TetraKCNG) are sperm-specific ion channels involved in sperm motility. Ancestral sequence reconstructions show that natural selection targeted the two genes in the brooding species. This may result from an adaptation to the novel environmental conditions surrounding sperm in the brooding species, either directly affecting sperm, or via an increase in male/female conflict. This phenomenon could have promoted prezygotic reproductive isolation between C3 and C5. Finally, the sperm receptors to egg chemoattractants differed between C3 and C5 in the ligand-binding region. We propose that mechanisms of species-specific gamete recognition in brittle stars occur during sperm chemotaxis (sperm attraction towards the eggs), contrary to other marine invertebrates where prezygotic barriers to interspecific hybridization typically occur before sperm-egg fusion.

亲缘关系密切的物种是探究生殖隔离（reproductive isolation）形成机制以及涵盖基因组层面的物种分化早期进程的关键研究模型。海蛇尾（brittle star）隐存物种复合群Ophioderma longicauda包含同域分布的体外产卵物种C3与体内育幼物种C5。本研究针对两种生殖模式迥异的近缘物种开展从头转录组测序（de novo transcriptome sequencing）与组装，以比较二者的遗传多样性（genetic diversity），并探究自然选择（natural selection）在生殖隔离形成中的作用。我们分别为C3和C5重构了20146和22123个基因，并鉴定得到12229个直系同源基因（orthologs）。C3的遗传多样性是C5的1.5至2倍，证实低亲本投入的物种具有更高水平的遗传多样性。48个基因在两物种的演化过程中受到正向多样化选择（positive diversifying selection）的靶向作用。值得注意的是，两个基因（NHE和TetraKCNG）为精子特异性离子通道（sperm-specific ion channels），参与精子活力（sperm motility）的调控。祖先序列重建（ancestral sequence reconstructions）结果显示，自然选择在育幼物种中靶向作用于这两个基因。这可能是为了适应育幼物种中精子所处的新型环境条件，该环境要么直接作用于精子，要么通过加剧雌雄冲突实现。该现象可能推动了C3与C5之间的合子前生殖隔离（prezygotic reproductive isolation）。最后，识别卵子化学引诱剂的精子受体在配体结合区域存在C3与C5之间的序列差异。我们提出，海蛇尾的物种特异性配子识别（gamete recognition）机制发生在精子趋化性（sperm chemotaxis，即精子向卵子的趋化吸引）阶段，这与其他海洋无脊椎动物不同，后者的种间杂交合子前障碍通常发生在精卵融合（sperm-egg fusion）之前。