Sex Pheromone Mediates Resource Partitioning Between Drosophila melanogaster and D. suzukii

Abstract

The spotted-wing drosophila, Drosophila suzukii and the cosmopolitan vinegar fly D. melanogaster feed on soft fruit and berries and widely overlap in geographic range. The presence of D. melanogaster reduces egg-laying in D. suzukii, possibly because D. melanogaster outcompetes D. suzukii larvae feeding in the same fruit substrate. Flies use pheromones to communicate for mating, but pheromones also serve a role in reproductive isolation between related species. We asked whether a D. melanogaster pheromone also modulates oviposition behaviour in D. suzukii. A dual-choice oviposition assay confirms that D. suzukii lays fewer eggs on blueberries exposed to D. melanogaster flies and further shows that female flies have a stronger effect than male flies. This was corroborated by treating berries with synthetic pheromones. Avoidance of D. suzukii oviposition is mediated by the female D. melanogaster pheromone (Z)-4-undecenal (Z4-11Al). Significantly fewer eggs were laid on berries treated with synthetic Z4-11Al. In comparison, the male pheromone (Z)-11-octadecenyl acetate (cVA) had no effect on D. suzukii oviposition. Z4-11Al is a highly volatile compound that is perceived via olfaction and it is accordingly behaviourally active at a distance from the source. D. suzukii is known to engage in mutual niche construction with the yeast Hanseniaspora uvarum, which strongly attracts flies. Adding Z4-11Al to fermenting H. uvarum significantly decreased D. suzukii flight attraction in a laboratory wind tunnel and a field trapping assay. That a D. melanogaster pheromone regulates oviposition in D. suzukii demonstrates that heterospecific pheromone communication contributes to reproductive isolation and resource partitioning in cognate species. Stimulo-deterrent diversion or push-pull methods, building on combined use of attractant and deterrent compounds, have shown promise for control of D. suzukii. A pheromone that specifically reduces D. suzukii attraction and oviposition adds to the toolbox for D. suzukii integrated management.