Data from: Drosophila pachea asymmetric lobes are part of a grasping device and stabilize one-sided mating

Background: Multiple animal species exhibit morphological asymmetries in male genitalia. In insects, left-right genital asymmetries evolved many times independently and have been proposed to appear in response to changes in mating position. However, little is known about the relationship between mating position and the interaction of male and female genitalia during mating, and functional analyses of asymmetric morphologies in genitalia are virtually non-existent. We investigated the relationship between mating position, asymmetric genital morphology and genital coupling in the fruit fly Drosophila pachea, in which males possess an asymmetric pair of external genital lobes and mate in an unusual right-sided position on top of the female. Results: We examined D. pachea copulation by video recording and by scanning electron microscopy of genital complexes. We observed that the interlocking of male and female genital organs in D. pachea is remarkably different from genital coupling in the well-studied D. melanogaster. In D. pachea, the female oviscapt valves are asymmetrically twisted during copulation. The male’s asymmetric lobes tightly grasp the female’s abdomen in an asymmetric ‘locking’ position, with the left and right lobes contacting different female structures. The male anal plates, which grasp the female genitalia in D. melanogaster, do not contact the female in D. pachea. Experimental lobe amputation by micro-surgery and laser-ablation of lobe bristles led to aberrant coupling of genitalia and variable mating positions, in which the male was tilted towards the right side of the female. Conclusion: We describe, for the first time, how the mating position depends on coupling of male and female genitalia in a species with asymmetric genitalia and one-sided mating position. Our results show that D. pachea asymmetric epandrial lobes do not act as a compensatory mechanism for the change from symmetric to one-sided mating position that occurred during evolution of D. pachea’s ancestors, but as holding devices with distinct specialized functions on the left and right sides.

研究背景：多种动物的雄性生殖器存在形态不对称现象。在昆虫类群中，左右生殖器不对称的特征多次独立演化，被认为是为适应交配体位的改变而演化产生。然而，目前学界对交配体位与交配过程中雌雄生殖器互作之间的关联知之甚少，针对生殖器不对称形态的功能研究也几乎空白。本研究以帕氏果蝇（Drosophila pachea）为研究对象，探讨了交配体位、生殖器不对称形态与生殖器耦合之间的关联。该物种的雄性拥有一对不对称的外生殖器叶，且会以罕见的右侧贴伏雌性背部的体位完成交配。

研究结果：我们通过视频录制以及生殖器复合体的扫描电子显微镜（scanning electron microscopy）观察，对帕氏果蝇的交配过程进行了分析。我们发现，帕氏果蝇雌雄生殖器的耦合方式与研究较为充分的黑腹果蝇（Drosophila melanogaster）存在显著差异。在帕氏果蝇交配过程中，雌性的产卵瓣会发生不对称扭转。雄性的不对称外生殖器叶会以不对称的“锁合”姿态紧密夹持雌性腹部，左右两侧的叶分别与雌性的不同结构接触。在黑腹果蝇中用于夹持雌性生殖器的雄性肛板，在帕氏果蝇中并未与雌性产生接触。通过显微手术切除外生殖器叶以及激光消融叶部刚毛的实验，导致了生殖器耦合异常以及交配体位异常，此时雄性会向雌性右侧倾斜。

研究结论：本研究首次阐明了在具有不对称生殖器与单侧交配体位的物种中，交配体位如何依赖于雌雄生殖器的耦合过程。我们的研究结果表明，帕氏果蝇的不对称下生殖板叶（epandrial lobes）并非用于补偿其祖先在演化历程中从对称交配体位转变为单侧交配体位的代偿结构，而是分别在左右两侧具备独特专属功能的夹持装置。