A shift to shorter cuticular hydrocarbons accompanies sexual isolation among Drosophila americana group populations.

Jeremy S Davis,Leonie C Moyle,Matthew J Pearcy,Joanne Y Yew

doi:10.1002/evl3.246

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 two populations of Drosophila americana (SC and NE) and one population of D. novamexicana, and dissect its underlying phenotypic and genetic mechanisms. Mating trials revealed strong sexual isolation between Drosophila novamexicana males and SC Drosophila americana females, as well as more moderate bi‐directional isolation between D. americana populations. Mating behavior data indicate SC D. americana males have the highest courtship efficiency and, unlike males of the other populations, 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 the SC D. americana population differs from the other populations primarily on the basis of compound carbon chain‐length. Moreover, manipulation of male CHC composition via heterospecific perfuming—specifically perfuming D. novamexicana males with SC D. americana males—abolishes their sexual isolation from these D. americana females. Of a set of candidates, a single gene—elongase CG17821—had patterns of gene expression consistent with a role in CHC differences between species. Sequence comparisons indicate D. novamexicana and our Nebraska (NE) D. americana population share a derived CG17821 truncation mutation that could also contribute to their shared “short” CHC phenotype. Together, these data suggest an evolutionary model for the origin and spread of this allele and its consequences for CHC divergence and sexual isolation in this group.

Highlights

Sensory signals can act as sexual cues that are critical for intraspecific mate evaluation and reproductive success
The copulation rate of SC D. americana females was significantly lower on average than both NE D. americana (P-adj = 0.025) and D. novamexicana (P-adj = 0.042), whereas NE D. americana and D. novamexicana females did not differ (P-adj = 0.15). These results indicate that SC D. americana females discriminate against heteropopulation males more strongly than do females of the other two populations, with the greatest discrimination against D. novamexicana males
We have demonstrated that sexual isolation between laboratory populations in the D. americana group is based on female choice of male chemical signals, and identified both the specific phenotypic shift between species in pheromone chemistry as well as a genetic variant likely contributing to this phenotypic change and the mating isolation that results from it

Summary

Introduction

Sensory signals can act as sexual cues that are critical for intraspecific mate evaluation and reproductive success Because they are frequently among the most rapidly evolving species differences (Smadja and Butlin 2009; Seddon et al 2013; Wilkins et al 2013), divergence in sensory sexual signals might often contribute to the earliest stages of reproductive isolation, in the form of prezygotic barriers between lineages (Butlin et al 2012; Ritchie 2007). Single genes contributing to species-specific CHC differences have been implicated as causes of reproductive isolation in several cases, including between D. melanogaster and D. simulans (desatF: Legendre et al 2008) and D. serrata and D. birchii (mFAS: Chung et al 2014) This framework provides an excellent resource for identifying candidate genes for sensory sexual signal variation in other Drosophila systems. Our data suggest that evolution of a male sexual signal—an overall shift in the relative abundance of longer versus shorter cuticular hydrocarbons, due to novel mutation in an elongase gene—has produced complete premating isolation between derived males and females from species that retain the ancestral trait and preference, as proposed in classical models (Kaneshiro 1976, 1980) of the evolution of asymmetric sexual isolation

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Results

Conclusion