Evolutionary shifts in taste coding in the fruit pest Drosophila suzukii.

Hany Km Dweck,John R Carlson,Wanyue Wang,Gaëlle Js Talross

doi:10.7554/elife.64317

Abstract

Although most Drosophila species lay eggs in overripe fruit, the agricultural pest Drosophila suzukii lays eggs in ripe fruit. We found that changes in bitter taste perception have accompanied this adaptation. We show that bitter-sensing mutants of Drosophila melanogaster undergo a shift in egg laying preference toward ripe fruit. D. suzukii has lost 20% of the bitter-sensing sensilla from the labellum, the major taste organ of the head. Physiological responses to various bitter compounds are lost. Responses to strawberry purées are lost from two classes of taste sensilla. Egg laying is not deterred by bitter compounds that deter other species. Profiling of labellar transcriptomes reveals reduced expression of several bitter Gr genes (gustatory receptors). These findings support a model in which bitter compounds in early ripening stages deter egg laying in most Drosophila species, but a loss of bitter response contributes to the adaptation of D. suzukii to ripe fruit.

Highlights

A major agricultural pest has recently emerged in dramatic fashion
We characterize the labellar transcriptomes of all three species and find that D. suzukii has reduced expression of a number of bitter taste receptor genes. These results provide an unprecedented view of how the bitter taste system of an invasive crop pest evolved in its shift to a new ecological niche
We examined the D. suzukii ovipositor by scanning electron microscopy (SEM) and identified four types of structures on each vaginal plate (VP): trichoid sensilla (TS), long bristles (LB), thorn bristles type I (TB1), and thorn bristles type 2 (TB2) (Figure 3—figure supplement 1; structures described in legend; terminology from Hodgkin and Bryant, 1978; Lauge, 1982)

Summary

Introduction

Drosophila suzukii, endemic to Southeast Asia, invaded California in 2008 (Hauser, 2011) It moved rapidly across the United States and has emerged in Northern Europe as well (Asplen et al, 2015; Cini et al, 2012; Depraet al., 2014; Dos Santos et al, 2017; Walsh et al, 2011). D. suzukii is a threat to a wide variety of fruit crops, including strawberries, blueberries, peaches, cherries, and grapes (Burrack et al, 2013; Lee et al, 2011; Mazzi et al, 2017) Whereas related species such as Drosophila melanogaster lay eggs in fermenting fruit that is of no commercial value, D. suzukii lays eggs in ripe fruit, leading to larval infestations and microbial infections that destroy crops (Karageorgi et al, 2017; Lee et al, 2011; Walsh et al, 2011). The study suggested the possibility that taste may play a role, a suggestion that we explore in the present study

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Conclusion