Editors' ChoiceSensory Perception

Rejecting the Wrong Mate

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Sci. Signal.  16 Jul 2013:
Vol. 6, Issue 284, pp. ec162
DOI: 10.1126/scisignal.2004513

The male fruit fly performs an elaborate courtship routine: First “singing” by vibrating his wings, then tapping of the female with his forelegs, in which reside chemosensory neurons, and “licking” the female’s abdomen with his proboscis (a mouth part). The foreleg tapping enables males to detect nonvolatile chemical cues on the cuticle of the potential mate that prevent mating with males. By selectively removing sensory body parts (antennae or maxillary paps), the distal part of the forelegs, or a portion of the mouth that included the proboscis or removing cues (keeping flies in the dark), Fan et al. determined that the foreleg tapping was required to prevent males from attempting to mate with females of different species. Using targeted genetic neuronal ablation, neurons with the gustatory receptor Gr32a or Gr33a, which are present in the forelegs, were required to prevent interspecies mating attempts. Genetic knockout of Gr32a or Gr33a revealed that loss of Gr32a resulted in interspecies mating attempts. Males court females lacking oenocytes, which are the cells that make the cuticle hydrocarbons. Fan et al. coated these oenocytes-lacking females with specific hydrocarbons and measured interspecies mating. They tested (i) z-7-tricosene, which is abundant on male Drosophila melanogaster and not on the females and is also abundant on the cuticles of two other Drosophila species, (ii) z-9-tricosene, and (iii)z-11-pentacosene, which are both abundant on another Drosophila species but not on D. melanogaster. Gr32a–/­– males, but not wild-type males, courted oenocytes-lacking D. melanogaster females coated with any of these hydrocarbons, suggesting that signaling by the Gr32a neurons is necessary to detect these chemical cues and prevent inappropriate mating behavior. Male D. melanogaster with a mutation in the FruM gene exhibited interspecies courtship behavior. Synaptic labeling studies suggested that Gr32a neurons did not directly synapse with FruM neurons, but knockdown studies indicated that FruM was necessary in the aDT6 subset of neurons to limit mating to conspecific females. Thus, Gr32a in the foreleg neurons is part of a neural circuit that includes the aDT6 FruM-positive neurons, and this circuit detects species-specific hydrocarbons on the female cuticle to prevent interspecies mating. As Koh and Carlson discuss, what remains to be determined is whether Gr32a, which is conserved among Drosophila species, functions as the receptor for the different hydrocarbons or whether there is a more divergent protein that serves as the chemoreceptor.

P. Fan, D. S. Maoli, O. M. Ahmed, Y. Chen, N. Agarwal, S. Kwong, A. G. Cai, J. Neitz, A. Renslo, B. S. Baker, N. M. Shah, Genetic and neural mechanisms that inhibit Drosophila from mating with other species. Cell 154, 89–102 (2013). [PubMed]

T.-W. Koh, J. R. Carlson, Interspecies sex and taste. Cell 154, 20–21 (2013). [PubMed]