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

Abstract

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 wildtype 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.

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

“…2a, Additional files 1 and 2). This mating angle did not differ significantly from the mean mating angle that we estimated from the raw data of our previous study [43] in wild-type males after 10–15 min of copulation (unpublished data; T -test: T 20  = 1.84, P =  0.080). The variance in mating angles was not equal between treatments (Bartlett’s test: K 2 2  = 13.15, P =  0.001).…”

“…In our video recordings, 17 % (3/18) of left lobe cut males and 11 % (2/18) of left lobe shaved males failed to mount the female at the first attempt while unmodified wildtype males never failed (0/16) (Additional file 1). In our previous study, the lobes of non-copulating mutant males were significantly smaller than those of copulating mutant males [43] and it was suggested that a critical lobe size might be required for efficient genitalia coupling. Indeed, the copulating ‘left-lobe cut’ males in this study had on average longer lobes than the non-copulating mutant males in our previous study (left: T 22.03  = −2.83, P =  0.010; right: T 9.14  = −7.43, P <  0.001), which corroborates this idea.…”

“…In this stock, about 20 % of the males possess short and bilaterally symmetric epandrial lobes (symmetric males) [43]. All flies came from the 15090.1698.02 stock except a few symmetric mutant males which came from a selection line that was derived from the 15090.1698.02 stock by selecting symmetric males for several generations in order to increase the proportion of symmetric males.…”

“…On each screenshot, a line was drawn between the bases of the wings in both the male and the female, and the angle between the two lines was measured using tpsDig 2.17 software [70]. The resulting angle is equivalent to the angle between the male’s and the female’s antero-posterior body axis as measured in our previous study [43] (Fig. 3a).…”

Coevolution between Male and Female Genitalia in the Drosophila melanogaster Species Subgroup

“…Experimental and genetic approaches have recently helped to understand the adaptive role of a few male grasping structures in Drosophila such as the mechanosensilla of the surstylus in D. melanogaster [64], the spine-like dorsal portion of the surstyli (known as secondary claspers) in D. bipectinata [65] and in D. ananassae [66], and the asymmetric epandrial lobes of D. pachea [67]. Alteration of these structures decreased male mating success, but the effect on female fitness was not determined.…”