Evolutionary shifts in taste coding in the fruit pest Drosophila suzukii

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.

Evolutionary divergence in sugar valuation shifts Drosophila suzukii oviposition choice towards ripe fruit

“…While we cannot exclude posi<onal effects of the transgenes, our func<onal analyses suggest that the reporters target a similar propor<on of sugar-GRNs in the two species. Thus D. suzukii appears to harbor less sugar-GRNs than D. melanogaster as reported also for bi$er-GRNs 21 . We cannot exclude that more subtle differences in the numbers of func<onally-dis<nct sugar-GRN subtypes exist between species.…”

“…We confirmed this overall reduction with a second independent insertion line (not shown). Although we cannot completely rule out positional insertion effects of the Gal4 transgenes, this might reflect a general reduction of GRN numbers in D. suzukii , as has been reported for bitter GRNs 21 . We also examined the axonal projections of GRNs labeled by DsuzGr64af-Gal4 in the central brain and confirmed that they project exclusively to the Sub-Esophageal Zone (SEZ), with arborization patterns highly reminiscent of those of the equivalent line in D. melanogaster ( Supplementary Fig.…”

“…To iden<fy the neuronal bases of inter-species divergent chemosensory responses, we first need to iden<fy the cri<cal molecules present in ripe and fermented substrates to which D. suzukii responds differently than other species. A recent study suggests that a reduc<on of D. suzukii's responses to bi$er compounds might have relieved an oviposi<on inhibi<on on ripe substrates 21 . Conversely, an increased response to fermenta<on by-products might have contributed to driving D. suzukii away from ro$en substrates 22 .…”

Which Sugar to Take and How Much to Take? Two Distinct Decisions Mediated by Separate Sensory Channels

“…In contrast, no GRNs expressing Gr61a-Gal4 ( Gr61a + GRNs) were identifiable in the labellar taste sensilla ( Figure 1B ). However, Dahanukar et al ( 2007 ), Weiss et al ( 2011 ), and Dweck et al ( 2021 ) reported the detection of a few Gr61a + GRNs in the labella, which might have escaped our detection. Comparisons of staining obtained with different Gr61a-Gal4 lines might help resolve this discrepancy.…”

Inter-species comparison of the orientation algorithm directing larval chemotaxis in the genus Drosophila

“…Endowed with a regular ovipositor, D. biarmipes is unable to reproduce on fresh fruits: it feeds on soft fermenting fruits. Multiple differences in chemosensory and mechanosensory behaviors have been reported between D. suzukii and D. biarmipes (Karageorgi, Bräcker et al 2017, Dweck, Talross et al 2021).…”