Sex-specific triacylglycerides are widely conserved in Drosophila and mediate mating behavior

Jacqueline SR Chin,Joanne Y Yew,Qi Ling Koh,Kenji Mori,Shane R Ellis,William J Etges,Stephen J Blanksby,Huong T Pham

doi:10.7554/elife.01751

Abstract

Pheromones play an important role in the behavior, ecology, and evolution of many organisms. The structure of many insect pheromones typically consists of a hydrocarbon backbone, occasionally modified with various functional oxygen groups. Here we show that sex-specific triacylclyerides (TAGs) are broadly conserved across the subgenus Drosophila in 11 species and represent a novel class of pheromones that has been largely overlooked. In desert-adapted drosophilids, 13 different TAGs are secreted exclusively by males from the ejaculatory bulb, transferred to females during mating, and function synergistically to inhibit courtship from other males. Sex-specific TAGs are comprised of at least one short branched tiglic acid and a long linear fatty acyl component, an unusual structural motif that has not been reported before in other natural products. The diversification of chemical cues used by desert-adapted Drosophila as pheromones may be related to their specialized diet of fermenting cacti.

Highlights

Chemical communication significantly influences many complex social behaviors, including aggression, kin recognition, and courtship (Wyatt, 2003)
In Drosophila, pheromones are produced by oenocytes and the male ejaculatory bulb and subsequently secreted onto the cuticular surface and anogenital region, respectively (Billeter et al, 2009; Yew et al, 2009)
To characterize the structures and functions of sex-specific TAGs, we focused on desert-adapted drosophilids from the D. repleta group, Drosophila arizonae and Drosophila mojavensis, two wellcharacterized models for speciation, reproductive isolation, and ecological studies (Ruiz et al, 1990; Markow, 1996; Etges and Jackson, 2001)

Summary

Introduction

Chemical communication significantly influences many complex social behaviors, including aggression, kin recognition, and courtship (Wyatt, 2003). The chemical structures and functions of insect pheromones have been intensely studied because of the fascinating diversity of behavioral properties and relevance to questions of speciation, reproductive isolation, and applications to pest control (Witzgall et al, 2010). Since the discovery of Bombykol in 1959 (Butenandt et al, 1959), hundreds of insect pheromones have been identified, including straight chain and branched alkanes and alkenes, oxygencontaining derivatives such as wax esters, fatty alcohols, and aldehydes, sterols, and isoprene-based compounds (Tillman et al, 1999; El-Sayed, 2012). Previous studies of Sophophora and Drosophila flies identified alkanes, alkenes, and oxygen-modified hydrocarbons as the major lipids used as pheromones (Jallon and David, 1987; Greenspan and Ferveur, 2000).

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