Evolution of a pest: towards the complete neuroethology of Drosophila suzukii and the subgenus Sophophora

Abstract

Comparative analysis of multiple genomes has been used extensively to examine the evolution of chemosensory receptors across the genus Drosophila. However, few studies have delved into functional characteristics, as most have relied exclusively on genomic data alone, especially for non-model species. In order to increase our understanding of olfactory evolution, we have generated a comprehensive assessment of the olfactory functions associated with the antenna and palps for Drosophila suzukii as well as several other members of the subgenus Sophophora, thus creating a functional olfactory landscape across a total of 20 species. Here we identify and describe several common elements of evolution, including consistent changes in ligand spectra as well as relative receptor abundance, which appear heavily correlated with the known phylogeny. We also combine our functional ligand data with protein orthologue alignments to provide a high-throughput evolutionary assessment and predictive model, where we begin to examine the underlying mechanisms of evolutionary changes utilizing both genetics and odorant binding affinities. In addition, we document that only a few receptors frequently vary between species, and we evaluate the justifications for evolution to reoccur repeatedly within only this small subset of available olfactory sensory neurons.

Evolution of olfactory circuits in insects

“…2c, d). This striking change was subsequently confirmed by other studies (Dekker et al 2006;Auer et al 2019;Keesey et al 2019; note ab2 sensilla are sometimes present in D. sechellia in very small numbers). Although the altered proportions have not yet been shown to directly affect behavior, it is telling that both neurons housed within the expanded ab3 sensillum population respond to noni odorants that attract D. sechellia, but are neutral or repellant to D. melanogaster and D. simulans (methyl hexanoate and 2-heptanone; Dekker et al 2006;Ibba et al 2010).…”

“…The ab3A neuron that shifted in D. sechellia also shows increased sensitivity to host-associated compounds in wild, ancestral populations of D. melanogaster that specialize on fallen marula fruit (Mansourian et al 2018; see also Shaw et al 2019) and in the distantly related D. suzukii that lays eggs on ripe fruit (Keesey et al 2015). Moreover, ab3A tuning was uniquely variable in a recent tour-de-force survey of odor responses in 10 OSN types across 20 Drosophila species (Keesey et al 2019). Most neurons showed conserved tuning across the clade, while ab3A flipped back and forth in whether it was most sensitive to methyl esters, ethyl esters, isobutyl acetate, or β-cyclocitral.…”

“…2c, d). Moreover, a broad electrophysiological survey of 20 Drosophila species showed shifting ratios of all three types of large basiconic sensilla across the genus (Keesey et al 2019). Species in the melanogaster subgroup tended to have the most ab3 (with D. sechellia and D. erecta representing extreme examples), spotted-wing species tended to have the most ab2, while still others were biased towards ab1.…”

“…Interestingly, these two IRs arose via tandem gene duplication ~ 50 million years ago and their resident neurons project to different compartments of the same glomerulus (Prieto-Godino et al 2017). ab3 sensilla in D. suzukii also comprise two putative subtypes (Keesey et al 2019). The situation evokes a process by which OSN and sensilla types are gained through the gradual acquisition of new receptors, patterning mechanisms and antennal lobe targets for a subset of previously uniform progenitor cells.…”

Evolution of olfactory receptors tuned to mustard oils in herbivorous Drosophilidae

“…The best-studied of these is Or22a, which has been evolutionarily lost by gene deletion in S. flava but not in S. pallida (19). In several drosophilids, Or22a is tuned to different ecologically relevant esters: ethyl-hexanoate in D. melanogaster (16), methylhexanoate in D. sechellia (42), 3-methyl-2-butenyl acetate in D. erecta (17), and isobutyl acetate in D. suzukii (43). Similarly, Ir75b is respectively tuned to butyric acid in D. melanogaster and to hexanoic acid in D. sechellia (15).…”