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：多种动物类群的雄性生殖器均存在形态不对称性。在昆虫中，生殖器左右不对称的性状已多次独立演化，且被认为是为应对交配体位变化而产生的适应性特征。然而，目前学界对交配体位与交配过程中雌雄生殖器互作的关联知之甚少，针对生殖器不对称形态的功能研究也几乎空白。本研究以潘氏果蝇（Drosophila pachea）为研究对象，该物种雄性拥有一对不对称的外生殖器叶，且会以罕见的雌性背侧右侧体位完成交配，旨在探究交配体位、生殖器不对称形态与生殖器锁合之间的关联。

研究结果：本研究通过视频录像及生殖器复合体的扫描电子显微镜（scanning electron microscopy）观察，对潘氏果蝇的交配过程进行了分析。研究发现，潘氏果蝇的雌雄生殖器锁合模式与被广泛研究的黑腹果蝇（Drosophila melanogaster）存在显著差异。交配过程中，雌性的产卵瓣（oviscapt valves）会发生不对称扭转；雄性的不对称外叶以不对称的“锁合”姿态紧紧夹持雌性腹部，左右两叶分别与雌性不同的结构接触；在黑腹果蝇中用于夹持雌性生殖器的雄性肛板，在潘氏果蝇中并未与雌性发生接触。通过显微手术切除外叶以及激光消融去除叶上刚毛的实验表明，该操作会导致生殖器锁合异常以及交配体位异常，雄性会向雌性右侧倾斜。

研究结论：本研究首次阐明了在生殖器不对称且采用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锁合过程。研究结果显示，潘氏果蝇的不对称第九背板叶（epandrial lobes）并非作为其祖先在演化过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发挥独特专一功能的夹持装置。