Evolution of a novel left-right asymmetry involving tissue remodelling and MyoID

Abstract

AbstractLeft-right asymmetries recurrently evolve in animals but the underlying developmental mechanisms are unknown. In mostDrosophilaspecies, the male genitalia is symmetric and undergoes a clockwise 360° rotation during development. InD. melanogaster, this tissue remodeling process is directed by class I myosins: in MyoID mutants the rotation is reversed and the genitalia remains symmetric. Males ofDrosophila pacheahave evolved unique left-right asymmetric genital organs and a characteristic right-sided copulation posture in the past 3-6 million years. To test if these asymmetries in morphology and behavior evolved via the recruitment of pre-existing directional cues controlled by MyoID, we used CRISPR to knockout MyoID inD. pachea. Strikingly, mutant males undergo a reverse genitalia rotation and develop mirror-image asymmetric genitalia, indicating that MyoID controls both the direction of genitalia rotation direction and morphological asymmetry. Although genital asymmetry is reversed, MyoID mutants still adopt a wild-type right-sided copulation posture. Our results show that MyoID and its asymmetry guidance role were recruited for the evolution of a novel left-right asymmetry inD. pacheaand that lateralized copulation behavior is determined by other mechanisms. The evolution of a new left-right organ size asymmetry inD. pacheainvolved recruitment of existing directional cues.