Data from: Distinct copulation positions in Drosophila pachea males with symmetric or asymmetric external genitalia

Left-right asymmetric genitalia have appeared multiple times independently in insects and have been associated with changes in mating positions. However, there is little experimental data on how the evolution of genital asymmetries may have affected the evolution of mating positions or vice versa. As opposed to its closely-related species, Drosophila pachea has a conspicuous asymmetry in its male genitalia external lobes, with the left lobe being 1.49 ± 0.08 (SD) times longer and thinner than the right lobe. In a laboratory stock, we found that 20% of the males possess fully symmetric lobes. To better understand how asymmetric genitalia may affect mating, we compared D. pachea copulation behaviour between these mutant males and wild-type males. We found that D. pachea wild-type males adopt a one-sided mating posture with the male always one-sided 8.55° ± 1.79° (SD) towards the female’s right side. Within 45-min recordings, all wild-type males did mate whereas 39% of symmetric mutants failed to form a stable mating complex and did not mate. In successful copulations, symmetric mutants also adopted a right-sided mating posture but the angle between male and female bodies was significantly more variable compared to wild-type males. Our results suggest that lobe size asymmetry is required for the formation of a stable mating complex and for the positioning of the male according to a precise angle on the female. However, lobe size asymmetry is not required for D. pachea right-sided mating posture.

左右不对称的生殖器在昆虫类群中多次独立演化形成，并与交配姿势的改变相关联。然而，目前关于生殖器不对称的演化如何影响交配姿势的演化，抑或交配姿势的演化如何反过来影响生殖器不对称演化的实验数据仍十分匮乏。与近缘物种不同，帕氏果蝇（Drosophila pachea）的雄性外生殖器叶存在显著不对称性：左叶的长度是右叶的1.49±0.08（标准差（standard deviation, SD））倍，且更为纤细。在一个实验室品系中，我们发现20%的雄性个体拥有完全对称的外生殖器叶。为了更好地探究不对称生殖器对交配行为的影响，我们对比了该对称突变雄性与野生型雄性的帕氏果蝇交配行为。结果显示，野生型雄性会采取单侧交配姿势，即雄性始终朝向雌性右侧，躯体偏角为8.55°±1.79°（SD）。在45分钟的记录时长内，所有野生型雄性均成功完成交配，而39%的对称突变雄性无法形成稳定的交配复合体，未能完成交配。在成功交配的对称突变雄性中，其同样采取了朝向右侧的交配姿势，但雌雄躯体间的夹角相较于野生型雄性显著更具变异性。我们的研究结果表明，外生殖器叶的大小不对称性是形成稳定交配复合体以及雄性按照精确角度在雌性躯体上完成定位的必要条件，但并非帕氏果蝇采取右侧朝向交配姿势的必要条件。