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.
Highlights
Multiple animal species exhibit morphological asymmetries in male genitalia
Ablation or shaving of the left epandrial lobe does not affect the mating sequence and its duration To assess the role of the left epandrial lobe, we either cut off part of the left lobe in wild-type males with surgical scissors under CO2-anaesthesia or we ablated all the bristles covering the left lobe with our laser ablation set-up
D. pachea male anal plates are not involved in grasping the female We found that male–female genital coupling in D. pachea is different from male–female genital coupling described in D. melanogaster and other species of the melanogaster species group
Summary
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. Several hypotheses for the evolution of asymmetric genitalia have been put forward, including space constraints, ecological pressures, antagonistic male–female coevolution and changes in mating positions [1, 2, 18, 19] Few of these have enjoyed sufficient support to be generally embraced, except maybe Huber's hypothesis that genitalia may become asymmetric in response to evolutionary changes in mating position [18]. A more complex formulation of Huber’s hypothesis would be that the first asymmetry that evolves is behavioral, which consequentially leads to multiple successive evolutionary changes in morphology and behavior which strengthen the asymmetry In this scenario, the evolutionary appearance of a fixed one-sided copulation position may affect genital function in at least three nonmutually exclusive ways: (1) right and left sides may change to morphologically compensate for the mismatch resulting from asymmetric contact between male and female genitalia; (2) right and left sides may start to assume different functions; (3) one side may lose its function and becomes reduced
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