The rise of a pest species represents a unique opportunity to address how species evolve new behaviors and adapt to novel ecological niches [1]. We address this question by studying the egg-laying behavior of Drosophila suzukii, an invasive agricultural pest species that has spread from Southeast Asia to Europe and North America in the last decade [2]. While most closely related Drosophila species lay their eggs on decaying plant substrates, D. suzukii oviposits on ripening fruit, thereby causing substantial economic losses to the fruit industry [3-8]. D. suzukii has evolved an enlarged, serrated ovipositor that presumably plays a key role by enabling females to pierce the skin of ripe fruit [9]. Here, we explore how D. suzukii selects oviposition sites, and how this behavior differs from that of closely related species. We have combined behavioral experiments in multiple species with neurogenetics and mutant analysis in D. suzukii to show that this species has evolved a specific preference for oviposition on ripe fruit. Our results also establish that changes in mechanosensation, olfaction, and presumably gustation have contributed to this ecological shift. Our observations support a model in which the emergence of D. suzukii as an agricultural pest is the consequence of the progressive modification of several sensory systems, which collectively underlie a radical change in oviposition behavior.

The ability to find and consume nutrient-rich diets for successful reproduction and survival is fundamental to animal life. Among the nutrients important for all animals are polyamines, a class of pungent smelling compounds required in numerous cellular and organismic processes. Polyamine deficiency or excess has detrimental effects on health, cognitive function, reproduction, and lifespan. Here, we show that a diet high in polyamine is beneficial and increases reproductive success of flies, and we unravel the sensory mechanisms that attract Drosophila to polyamine-rich food and egg-laying substrates. Using a combination of behavioral genetics and in vivo calcium imaging, we demonstrate that Drosophila uses multisensory detection to find and evaluate polyamines present in overripe and fermenting fruit, their favored feeding and egg-laying substrate. In the olfactory system, two coexpressed ionotropic receptors (IRs), IR76b and IR41a, mediate the long-range attraction to the odor. In the gustatory system, multimodal taste sensation by IR76b receptor and GR66a bitter receptor neurons is used to evaluate quality and valence of the polyamine providing a mechanism for the fly’s high attraction to polyamine-rich and sweet decaying fruit. Given their universal and highly conserved biological roles, we propose that the ability to evaluate food for polyamine content may impact health and reproductive success also of other animals including humans. Animals, including humans, evaluate food by its smell and taste. Odors and tastes not only signal the presence of food, they also reveal details about the type and amount of nutrients contained in it. A preference for certain foods frequently reflects the specific metabolic needs of an animal. Among the important but less known compounds that animals consume with their diet are polyamines. These pungent smelling molecules are essential for reproduction, development, and cognition. Interestingly, they are also produced by the cell and body, but their levels decline with age. A diet high in polyamines can improve age-related memory deficits and loss of fertility. We have used the model fly Drosophila melanogaster to unravel if and how animals detect polyamines in their food and environment, and which role this detection plays in their food choice behavior. Polyamine levels are particularly high in the fly’s favorite food and egg-laying substrate, overripe and decaying fruit. We found that food supplemented with polyamines indeed improves the reproductive success of a fly couple. We show that Drosophila is highly attracted to polyamines and uses them to identify promising egg-laying and feeding sites. It detects them through an ancient clade of receptor proteins on its olfactory and taste organs. We speculate that other animals can also detect polyamines and use their smell and taste to identify sources of these beneficial nutrients.