Rhebergen Flor T, Courtier-Orgogozo Virginie, Dumont Julien, Schilthuizen Menno, Lang Michael
Naturalis Biodiversity Center, Darwinweg 2, 2333 CR, Leiden, The Netherlands.
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, 1098 XH, Amsterdam, The Netherlands.
BMC Evol Biol. 2016 Sep 1;16(1):176. doi: 10.1186/s12862-016-0747-4.
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.
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.
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.
多种动物物种的雄性生殖器存在形态不对称现象。在昆虫中，左右生殖器不对称多次独立进化，有人提出这是对交配姿势变化的响应。然而，关于交配姿势与交配过程中雌雄生殖器相互作用之间的关系，人们知之甚少，而且对生殖器不对称形态的功能分析几乎不存在。我们研究了果蝇帕切亚（Drosophila pachea）的交配姿势、不对称生殖器形态与生殖器耦合之间的关系，在该果蝇中，雄性拥有一对不对称的外部生殖器叶，且在雌性上方以不寻常的右侧姿势进行交配。
我们通过视频记录和生殖器复合体的扫描电子显微镜检查了帕切亚果蝇的交配过程。我们观察到，帕切亚果蝇中雌雄生殖器的连锁与研究充分的黑腹果蝇（D. melanogaster）的生殖器耦合显著不同。在帕切亚果蝇中，雌性产卵器瓣在交配时不对称扭曲。雄性的不对称叶以不对称的“锁定”姿势紧紧抓住雌性的腹部，左右叶接触不同的雌性结构。在黑腹果蝇中抓住雌性生殖器的雄性肛板，在帕切亚果蝇中不与雌性接触。通过显微手术对叶进行截肢以及用激光烧蚀叶上的刚毛，导致生殖器异常耦合和可变的交配姿势，其中雄性向雌性右侧倾斜。
我们首次描述了在一个具有不对称生殖器和单侧交配姿势的物种中，交配姿势如何依赖于雌雄生殖器的耦合。我们的结果表明，帕切亚果蝇不对称的尾叶并不作为一种补偿机制，用于补偿在帕切亚果蝇祖先进化过程中从对称交配姿势到单侧交配姿势的变化，而是作为具有左右两侧不同专门功能的固定装置。
