Chemical Cues that Guide Female Reproduction in Drosophila melanogaster

Abstract

Chemicals released into the environment by food, predators and conspecifics play critical roles in Drosophila reproduction. Females and males live in an environment full of smells, whose molecules communicate to them the availability of food, potential mates, competitors or predators. Volatile chemicals derived from fruit, yeast growing on the fruit, and flies already present on the fruit attract Drosophila, concentrating flies at food sites, where they will also mate. Species-specific cuticular hydrocarbons displayed on female Drosophila as they mature are sensed by males and act as pheromones to stimulate mating by conspecific males and inhibit heterospecific mating. The pheromonal profile of a female is also responsive to her nutritional environment, providing an honest signal of her fertility potential. After mating, cuticular and semen hydrocarbons transferred by the male change the female’s chemical profile. These molecules make the female less attractive to other males, thus protecting her mate’s sperm investment. Females have evolved the capacity to counteract this inhibition by ejecting the semen hydrocarbon (along with the rest of the remaining ejaculate) a few hours after mating. Although this ejection can temporarily restore the female’s attractiveness, shortly thereafter another male pheromone, a seminal peptide, decreases the female’s propensity to re-mate, thus continuing to protect the male’s investment. Females use olfaction and taste sensing to select optimal egg-laying sites, integrating cues for the availability of food for her offspring, and the presence of other flies and of harmful species. We argue that taking into account evolutionary considerations such as sexual conflict, and the ecological conditions in which flies live, is helpful in understanding the role of highly species-specific pheromones and blends thereof, as well as an individual’s response to the chemical cues in its environment.

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Acknowledgements

We thank the editors Etya Amsalem and Abraham Hefetz for the opportunity to write this review, Frank Avila, Andrea Vogel, and two anonymous reviewers for helpful comments on the manuscript, and NIH grants R01-HD038921 and R01-HD059060 to MFW, and MFW and AG Clark (respectively) for support.

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Correspondence to Jean-Christophe Billeter or Mariana F. Wolfner.

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Billeter, JC., Wolfner, M.F. Chemical Cues that Guide Female Reproduction in Drosophila melanogaster. J Chem Ecol 44, 750–769 (2018). https://doi.org/10.1007/s10886-018-0947-z

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Keywords

  • Reproduction
  • Pheromones
  • Chemical cues
  • Drosophila
  • Seminal fluid proteins
  • Olfaction
  • Gustation