Neuropeptides Modulate Female Chemosensory Processing upon Mating in Drosophila

Abstract

A female’s reproductive state influences her perception of odors and tastes along with her changed behavioral state and physiological needs. The mechanism that modulates chemosensory processing, however, remains largely elusive. Using Drosophila, we have identified a behavioral, neuronal, and genetic mechanism that adapts the senses of smell and taste, the major modalities for food quality perception, to the physiological needs of a gravid female. Pungent smelling polyamines, such as putrescine and spermidine, are essential for cell proliferation, reproduction, and embryonic development in all animals. A polyamine-rich diet increases reproductive success in many species, including flies. Using a combination of behavioral analysis and in vivo physiology, we show that polyamine attraction is modulated in gravid females through a G-protein coupled receptor, the sex peptide receptor (SPR), and its neuropeptide ligands, MIPs (myoinhibitory peptides), which act directly in the polyamine-detecting olfactory and taste neurons. This modulation is triggered by an increase of SPR expression in chemosensory neurons, which is sufficient to convert virgin to mated female olfactory choice behavior. Together, our data show that neuropeptide-mediated modulation of peripheral chemosensory neurons increases a gravid female’s preference for important nutrients, thereby ensuring optimal conditions for her growing progeny.

Abstract

During pregnancy, women frequently report that their food preferences change—sometimes dramatically. This study unravels a mechanism that changes a mated female’s perception of odors and tastes and thereby adapts her food choices to her reproductive state.

Author Summary

Food choices often correlate with nutritional needs or physiological states of an animal. For instance, during pregnancy, women frequently report that their food preferences change—sometimes dramatically. In part, this change in preference is brought about by a change in the perception of smells and tastes. Research has shown that female insects also change their food and egg-laying site preferences depending on their reproductive state. However, the mechanisms that trigger these changes are not understood in either mammals or insects. We have unraveled a mechanism that changes a mated female’s perception of odors and tastes and thereby adapts her choices to her reproductive state. Using the model fly Drosophila melanogaster, we show that mating increases females’ interest in sources of specific beneficial nutrients: polyamines such as spermine and putrescine. Polyamine levels in the body are maintained by diet, microorganisms in the gut, and own synthesis. Increased levels are required during pregnancy and reproduction. Indeed, mated females were more attracted to the taste and smell of polyamines than virgins were. We found that this behavioral modulation is regulated through a secreted peptide and its receptor, whose expression rises markedly in sensory organs upon mating. This signal appears to change the intensity of how polyamine taste or smell information reaches the brain and ultimately elicits a choice. Given that odor and taste processing in mammals and insects are similar, our findings in flies can lead to a better understanding of how dynamic physiological states affect our perception of the environment and lead us to adapt our choices of food and other relevant decisions.