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Introduction Male genitalia are thought to ensure transfer of sperm through direct physical contact with female during copulation. However, little attention has been given to their pre-copulatory role with respect to sexual selection and sexual conflict. Males of the fruitfly Drosophila pachea have a pair of asymmetric external genital lobes, which are primary sexual structures and stabilize the copulatory complex of female and male genitalia. We wondered if genital lobes in D. pachea may have a role before or at the onset of copulation, before genitalia contacts are made. Results We tested this hypothesis with a D. pachea stock where males have variable lobe lengths. In 92 mate competition trials with a single female and two males, females preferentially engaged into a first copulation with males that had a longer left lobe and that displayed increased courtship vigor. In 53 additional trials with both males having partially amputated left lobes of different lengths, we observed a weaker and non-significant effect of left lobe length on copulation success. Courtship durations significantly increased with female age and when two males courted the female simultaneously, compared to trials with only one courting male. In addition, lobe length did not affect sperm transfer once copulation was established. Conclusion Left lobe length affects the chance of a male to engage into copulation. The morphology of this primary sexual trait may affect reproductive success by mediating courtship signals or by facilitating the establishment of genital contacts at the onset of copulation.

Male genitalia are thought to ensure transfer of sperm through direct physical contact with female during copulation. Such primary sexual traits were also observed to affect pre-copulatory female mate-choice in some Vertebrates species, but whether this also occurs in insects is unknown. Males of the fruitfly Drosophila pachea have a pair of asymmetric external genital lobes, which are primary sexual structures and stabilize the copulatory complex of female and male genitalia. We tested for a pre-copulatory courtship role of these lobes with a D. pachea stock where males have variable lobe lengths. In 111 mate competition experiments with a single female and two males, females preferentially engaged into a first copulation with males that had a longer left lobe. Courtship durations increased with female age and when two males courted the female simultaneously, compared to experiments with only one courting male. In 54 additional experiments with both males having partially amputated left lobes, we observed a similar but weaker effect of left lobe length on copulation success. We conclude that left lobe length affects male mating success before genital contact. Our results suggest that primary male sexual traits in insects can serve as a signal for pre-copulatory mate-choice.

How novel left-right asymmetries evolve in animals is unknown. Drosophila pachea males display a unique left-right asymmetry in the genital organs and mate in a right-sided position onto the female. In flies, male genitalia undergo a clockwise 360° rotation during development. To test if this tissue remodeling process is linked to asymmetry development in the male genitalia of Drosophila pachea, we developed CRIPSR and transgenesis in this singular species. As in D. melanogaster, mutants of the MyoID gene homolog undergo reverse rotation of the developing genitalia. In addition, they have mirror-image asymmetric genitalia. Although their genital asymmetry is reversed mutants still adopt a right-sided copulation posture. Our results reveal a novel mechanism for establishing left-right asymmetry in animals, involving complex tissue remodeling and MyoID.