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

Abstract

BackgroundMultiple 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.ResultsWe 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.ConclusionWe 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0747-4) contains supplementary material, which is available to authorized users.

The evolution of asymmetric genitalia in Coleoptera

“…However, a much more comprehensive sampling of the Cholevini, as well as functional and experimental studies are needed to confirm this. For example, synchrotron micro-CT scanning of snap-frozen copulations (as we are currently performing in Drosophila pachea , a dipteran species with asymmetric male genitalia [34]) may reveal the effect of genital asymmetry on sperm transfer. Unlike Diptera, Coleoptera usually have a single unpaired spermatheca, but nevertheless there may be internal female asymmetries involved in female sperm storage control that the male's asymmetric sperm delivery apparatus may help to bypass.…”

Fitness advantages of the biased use of paired laterally symmetrical penises in an insect

“…In contrast, ablation of the right process, which is less developed than the left one, does not affect this measure of male reproductive success compared with unmanipulated controls (Tsuchiya & Hayashi, ). An exceptional case has been reported for the male genitalia of Drosophila pachea : ablation of either the right or left male genital lobe (epandrial lobes), in which the left lobe is much longer than the right, resulted in abnormal male positions during mating with equal frequency (Rhebergen, Courtier‐Orgogozo, Dumont, Schilthuizen, & Lang, ). However, the precise positions of each lobe and mating angle between the male and female bodies were different between the two treatments (Rhebergen et al., ), indicating a possible effect on male reproductive success.…”

“…p-values shown above the bars are results after correction for multiple comparisons using FDR. Error bars indicate the 95% confidence intervals positions during mating with equal frequency(Rhebergen, Courtier-Orgogozo, Dumont, Schilthuizen, & Lang, 2016). However, the precise positions of each lobe and mating angle between the male and female bodies were different between the two treatments(Rhebergen et al, 2016), indicating a possible effect on male reproductive success.…”

Repeated evolution of asymmetric genitalia and right-sided mating behavior in theDrosophila nannopteraspecies group

“…The four species separated about 3-6 Ma and lineage-specific changes likely led to the distinct and elaborated asymmetries in each species [28]. Interestingly, D. pachea mates in a right-sided copulation position where the male rests on top of the female abdomen with its antero-posterior midline shifted about 6-8 degrees to the right side of the female midline [26, 29]. This one-sided mating posture is associated with asymmetric coupling of female and male genitalia during copulation, with the male genital arch being rotated about 6 degrees towards the female’s right side.…”