Evolution of Multiple Sensory Systems Drives Novel Egg-Laying Behavior in the Fruit Pest Drosophila suzukii

Abstract

The rise of a pest species represents a unique opportunity to address how species evolve new behaviors and adapt to novel ecological niches [1Gould F. The evolutionary potential of crop pests.Am. Sci. 1991; 79: 496-507Google Scholar]. 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 [2Fraimout A. Debat V. Fellous S. Hufbauer R.A. Foucaud J. Pudlo P. Marin J.-M. Price D.K. Cattel J. Chen X. et al.Deciphering the routes of invasion of Drosophila suzukii by means of ABC random forest.Mol. Biol. Evol. 2017; (Published online January 24, 2017)https://doi.org/10.1093/molbev/msx050Crossref PubMed Scopus (102) Google Scholar]. 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 [3Bolda M.P. Goodhue R.E. Zalom F.G. Spotted wing Drosophila: potential economic impact of a newly established pest.Agric. Resource Econ. Update, Univ. Calif. Giannini Foundation Agric. Econ. 2010; 13: 5-8Google Scholar, 4Burrack H.J. Fernandez G.E. Spivey T. Kraus D.A. Variation in selection and utilization of host crops in the field and laboratory by Drosophila suzukii Matsumara (Diptera: Drosophilidae), an invasive frugivore.Pest Manag. Sci. 2013; 69: 1173-1180Crossref PubMed Scopus (185) Google Scholar, 5Cini A. Anfora G. Escudero-Colomar L.A. Grassi A. Santosuosso U. Seljak G. Papini A. Tracking the invasion of the alien fruit pest Drosophila suzukii in Europe.J. Pest Sci. 2014; 87: 559-566Crossref Scopus (170) Google Scholar, 6Ioriatti C. Walton V. Dalton D. Anfora G. Grassi A. Maistri S. Mazzoni V. Drosophila suzukii (Diptera: Drosophilidae) and its potential impact to wine grapes during harvest in two cool climate wine grape production regions.J. Econ. Entomol. 2015; 108: 1148-1155Crossref PubMed Scopus (117) Google Scholar, 7Rota-Stabelli O. Blaxter M. Anfora G. Drosophila suzukii.Curr. Biol. 2013; 23: R8-R9Abstract Full Text Full Text PDF PubMed Scopus (112) Google Scholar, 8Keesey I.W. Knaden M. Hansson B.S. Olfactory specialization in Drosophila suzukii supports an ecological shift in host preference from rotten to fresh fruit.J. Chem. Ecol. 2015; 41: 121-128Crossref PubMed Scopus (153) Google Scholar]. D. suzukii has evolved an enlarged, serrated ovipositor that presumably plays a key role by enabling females to pierce the skin of ripe fruit [9Atallah J. Teixeira L. Salazar R. Zaragoza G. Kopp A. The making of a pest: the evolution of a fruit-penetrating ovipositor in Drosophila suzukii and related species.Proc. Biol. Sci. 2014; 281: 20132840Crossref PubMed Scopus (235) Google Scholar]. 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.