Abstract

Insects use sex pheromones as a reproductive isolating mechanism to attract conspecifics and repel heterospecifics. Despite the profound knowledge of sex pheromones, little is known about the coevolutionary mechanisms and constraints on their production and detection. Using whole-genome sequences to infer the kinship among 99 drosophilids, we investigate how phylogenetic and chemical traits have interacted at a wide evolutionary timescale. Through a series of chemical syntheses and electrophysiological recordings, we identify 52 sex-specific compounds, many of which are detected via olfaction. Behavioral analyses reveal that many of the 43 male-specific compounds are transferred to the female during copulation and mediate female receptivity and/or male courtship inhibition. Measurement of phylogenetic signals demonstrates that sex pheromones and their cognate olfactory channels evolve rapidly and independently over evolutionary time to guarantee efficient intra- and inter-specific communication systems. Our results show how sexual isolation barriers between species can be reinforced by species-specific olfactory signals.

Highlights

  • Insects use sex pheromones as a reproductive isolating mechanism to attract conspecifics and repel heterospecifics

  • We investigated the relationships of 99 species within the family Drosophilidae, 95 of which span the diversity of flies across the genus Drosophila (2–3 species per eachgroup)

  • That our analysis focuses on the at[1] and at[4] sensilla that have been shown to be involved in the detection of volatile pheromones in D. melanogaster and close relatives[24,32,51,52], as well as in D. mojavensis[22]

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Summary

Introduction

Insects use sex pheromones as a reproductive isolating mechanism to attract conspecifics and repel heterospecifics. Related species tend to use different pheromone blends of shared chemical compounds as a result of genetic similarities and biosynthetic pathways shared by ancestry[7,8,9] This diversity in sex pheromone communication can become further affected by factors like geographical or host variations. Olfactory sexual communication in D. melanogaster is arguably one of the best-studied systems in animals[28], and is carried out through limited chemical signals, including cis-vaccenyl acetate (cVA)[29]. This compound is produced exclusively by males and transferred to females during copulation, which reduces the attractiveness of the freshly mated females[30]. Despite the profound knowledge of cVA-induced behaviors in D. melanogaster, little is known about analogous stimuli that regulate social and sexual behaviors in other drosophilids

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