Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.
Howard Hughes Medical Institute, Chevy Chase, MD, USA.
Genome Biol Evol. 2024 Jul 3;16(7). doi: 10.1093/gbe/evae118.
Ovaries play key roles in fitness and evolution: they are essential female reproductive structures that develop and house the eggs in sexually reproducing animals. In Drosophila, the mature ovary contains multiple tubular egg-producing structures known as ovarioles. Ovarioles arise from somatic cellular structures in the larval ovary called terminal filaments (TFs), formed by TF cells and subsequently enclosed by sheath (SH) cells. As in many other insects, ovariole number per female varies extensively in Drosophila. At present, however, there is a striking gap of information on genetic mechanisms and evolutionary forces that shape the well-documented rapid interspecies divergence of ovariole numbers. To address this gap, here we studied genes associated with Drosophila melanogaster ovariole number or functions based on recent experimental and transcriptional datasets from larval ovaries, including TFs and SH cells, and assessed their rates and patterns of molecular evolution in five closely related species of the melanogaster subgroup that exhibit species-specific differences in ovariole numbers. From comprehensive analyses of protein sequence evolution (dN/dS), branch-site positive selection, expression specificity (tau), and phylogenetic regressions (phylogenetic generalized least squares), we report evidence of 42 genes that showed signs of playing roles in the genetic basis of interspecies evolutionary change of Drosophila ovariole number. These included the signaling genes upd2 and Ilp5 and extracellular matrix genes vkg and Col4a1, whose dN/dS predicted ovariole numbers among species. Together, we propose a model whereby a set of ovariole-involved gene proteins have an enhanced evolvability, including adaptive evolution, facilitating rapid shifts in ovariole number among Drosophila species.
它们是雌性生殖结构的重要组成部分，在有性繁殖的动物中发育和容纳卵子。在果蝇中，成熟的卵巢包含多个称为卵巢小管的管状卵子产生结构。卵巢小管由称为终端丝 (TF) 的幼虫卵巢中的体细胞结构产生，由 TF 细胞形成，随后被鞘 (SH) 细胞包围。与许多其他昆虫一样，果蝇中每个雌性的卵巢小管数量差异很大。然而，目前对于塑造卵巢小管数量在物种间迅速分化的遗传机制和进化力量，存在着惊人的信息差距。为了解决这一差距，我们在这里根据幼虫卵巢的最新实验和转录数据集，研究了与果蝇卵巢小管数量或功能相关的基因，包括 TF 和 SH 细胞，并评估了它们在五个密切相关的黑腹果蝇亚组物种中的分子进化率和模式，这些物种在卵巢小管数量上表现出物种特异性差异。通过对蛋白质序列进化 (dN/dS)、分支位点正选择、表达特异性 (tau) 和系统发育回归 (系统发育广义最小二乘法) 的综合分析，我们报告了 42 个基因的证据，这些基因表明在果蝇卵巢小管数量的种间进化变化的遗传基础中发挥作用。这些基因包括信号基因 upd2 和 Ilp5 以及细胞外基质基因 vkg 和 Col4a1，它们的 dN/dS 预测了物种间的卵巢小管数量。总之，我们提出了一个模型，即一组涉及卵巢小管的基因蛋白具有增强的可进化性，包括适应性进化，从而促进了果蝇物种间卵巢小管数量的快速变化。
