A shift to shorter cuticular hydrocarbons accompanies sexual isolation amongDrosophila americanagroup populations

Abstract

Because sensory signals often evolve rapidly, they could be instrumental in the emergence of reproductive isolation between species. However, pinpointing their specific contribution to isolating barriers, and the mechanisms underlying their divergence, remains challenging. Here we demonstrate sexual isolation due to divergence in chemical signals between members of the Drosophila americana group, dissect its underlying phenotypic and genetic mechanisms, and propose a model of its evolutionary history. Mating trials revealed complete sexual isolation between Drosophila novamexicana males and Drosophila americana texana females, as well as more moderate bi-directional isolation between D. americana subspecies. Mating behavior recordings indicate D. a. texana males have the highest courtship efficiency and, unlike males of the other two species, are accepted by females of all species. Quantification of cuticular hydrocarbon (CHC) profiles, chemosensory signals that are used for species recognition and mate finding in Drosophila, shows that D. a. texana differs from the other two species primarily on the basis of compound carbon chain-length. Moreover, manipulation of male CHC composition via heterospecific perfuming—specifically perfuming D. novamexicana males with D. a. texana males—abolishes their sexual isolation from D. a. texana females. Evaluation of candidate genes for patterns of gene expression reveals a single gene—elongase CG17821—with patterns consistent with a causal role in CHC differences between species. Sequence comparisons indicate D. novamexicana and D. a. americana share a derived CG17821 truncation mutation that could also contribute to their shared “short” CHC phenotype. We present an evolutionary model for the origin and spread of this allele and the consequences for CHC divergence and sexual isolation in this group.

The female pheromone (Z)-4-undecenal mediates flight attraction and courtship in Drosophila melanogaster

“…Drosophila cuticular hydrocarbon (CHC) profiles are sexually dimorphic, they vary and rapidly diverge between species and therefore contribute to sexual, reproductive isolation (Howard et al 2003, Legendre et al 2008, Alves et al 2010, De Oliveira et al 2011, Davis et al 2020. Naturally, this congruently applies to their volatile oxidation products, particularly monounsaturated aldehydes, which derive from diunsaturated CHCs.…”