Repeated evolution of asymmetric genitalia and right-sided mating behavior in the Drosophila nannoptera species group

Andrea E Acurio,Flor T Rhebergen,Virginie Courtier-Orgogozo,Michael Lang,Sarah Paulus

doi:10.1186/s12862-019-1434-z

Abstract

BackgroundMale genitals have repeatedly evolved left-right asymmetries, and the causes of such evolution remain unclear. The Drosophila nannoptera group contains four species, among which three exhibit left-right asymmetries of distinct genital organs. In the most studied species, Drosophila pachea, males display asymmetric genital lobes and they mate right-sided on top of the female. Copulation position of the other species is unknown.ResultsTo assess whether the evolution of genital asymmetry could be linked to the evolution of one-sided mating, we examined phallus morphology and copulation position in D. pachea and closely related species. The phallus was found to be symmetric in all investigated species except D. pachea, which displays an asymmetric phallus with a right-sided gonopore, and D. acanthoptera, which harbors an asymmetrically bent phallus. In all examined species, males were found to position themselves symmetrically on top of the female, except in D. pachea and D. nannoptera, where males mated right-sided, in distinctive, species-specific positions. In addition, the copulation duration was found to be increased in the nannoptera group species compared to closely related outgroup species.ConclusionOur study shows that gains, and possibly losses, of asymmetry in genital morphology and mating position have evolved repeatedly in the nannoptera group. Current data does not allow us to conclude whether genital asymmetry has evolved in response to changes in mating position, or vice versa.

Highlights

Male genitals have repeatedly evolved left-right asymmetries, and the causes of such evolution remain unclear
We examined the aedeagus of two dissected D. pachea males using scanning electron microscopy (SEM) and found that both were strikingly asymmetric (Fig. 1)
Our previous data from D. pachea [26, 29] was re-analyzed in this study with a Asymmetry in mating position and in phallus have evolved in different branches of the nannoptera group phylogeny Across the nannoptera group, we find no striking correspondence between right-sided mating posture and asymmetric male genitalia

Summary

Introduction

Male genitals have repeatedly evolved left-right asymmetries, and the causes of such evolution remain unclear. The Drosophila nannoptera group contains four species, among which three exhibit left-right asymmetries of distinct genital organs. In the most studied species, Drosophila pachea, males display asymmetric genital lobes and they mate right-sided on top of the female. New behaviors can initiate secondary evolutionary shifts in morphology, physiology or ecology (“behavioral drive”) [1,2,3,4,5,6,7,8,9], for example when they bring an organism into contact with new environmental factors. The evolution of left-right asymmetric genitalia in insects is a case where morphology was proposed to have evolved in response to changes in mating behavior [17]. While most extant insect species copulate with the male being on top of the female abdomen, the ancestral mating position in insects is inferred to be a configuration with the female on top of the male [18, 20, 21]

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