Evolutionary Insights into Taste Perception of the Invasive PestDrosophila suzukii

Abstract

Chemosensory perception allows insects to interact with the environment by perceiving odorant or tastant molecules; genes encoding chemoreceptors are the molecular interface between the environment and the insect, and play a central role in mediating its chemosensory behavior. Here, we explore how the evolution of these genes in the emerging pest Drosophila suzukii correlates with the peculiar ecology of this species. We annotated approximately 130 genes coding for gustatory receptors (GRs) and divergent ionotropic receptors (dIRs) in D. suzukii and in its close relative D. biarmipes. We then analyzed the evolution, in terms of size, of each gene family as well of the molecular evolution of the genes in a 14 Drosophila species phylogenetic framework. We show that the overall evolution of GRs parallels that of dIRs not only in D. suzukii, but also in all other analyzed Drosophila. Our results reveal an unprecedented burst of gene family size in the lineage leading to the suzukii subgroup, as well as genomic changes that characterize D. suzukii, particularly duplications and strong signs of positive selection in the putative bitter-taste receptor GR59d. Expression studies of duplicate genes in D. suzukii support a spatio-temporal subfunctionalization of the duplicate isoforms. Our results suggest that D. suzukii is not characterized by gene loss, as observed in other specialist Drosophila species, but rather by a dramatic acceleration of gene gains, compatible with a highly generalist feeding behavior. Overall, our analyses provide candidate taste receptors specific for D. suzukii that may correlate with its specific behavior, and which may be tested in functional studies to ultimately enhance its control in the field.

Sex‐biased gene expression in antennae of Drosophila suzukii

“…We additionally analyzed differentially‐expressed genes focusing on a variety of chemosensory genes. First, we searched for the full repertoire of various chemosensory gene families according to previous studies (Crava et al, 2016; Hickner et al, 2016; Karageorgi et al, 2017; Ometto et al, 2013; Ramasamy et al, 2016), and then compared their expression levels between male and FA among the “antennae‐enriched” genes. The normalized gene expression levels of the chemosensory genes were plotted between MA and FA, showing their overall distribution (Figure 3a), and the number of sex‐biased chemosensory genes are shown in Figure 3b.…”

“…The other IRs including divergent IRs were not significantly different between two sexes (Table S9). Unlike ORs, no sex‐biased GRs and IRs in D. suzukii were found in its close relative species (Crava et al, 2016). The results indicate that the evolutional process of these receptors could be paralleled not only in D. suzukii , but also in other Drosophila members.…”

“…The candidate transcripts were further assembled with corresponding genome scaffolds downloaded from the SpottedWingFlyBase (Chiu et al, 2013) to verify exon‐intron boundaries. Previously curated gene models either from the North American strain (Hickner et al, 2016) or from the Italian strain (Crava et al, 2016; Ramasamy et al, 2016) of D. suzukii were compared to confirm the start and stop codons and to give appropriate names.…”

“…D. suzukii , known as spotted‐wing drosophila, is a native from Southeast Asia, and has successfully spread to all other continents, becoming a serious pest of the small and stone fruits in America and Europe (Lee et al, 2011a, 2011b; Rota‐Stabelli, Blaxter, & Anfora, 2013). The fly's ability to cause large‐scale economic loss is closely related to its morphological and biochemical adaptations, and subsequent ecological shifting for food resources (Crava, Ramasamy, Ometto, Anfora, & Rota‐Stabelli, 2016; Hickner et al, 2016; Keesey et al, 2015; Nguyen et al, 2016; Revadi et al, 2015). Unlike other members of Drosophilidae, D. suzukii has evolved a preference for fresh and ripening fruits (Rota‐Stabelli et al, 2013), due to a new found “attraction” toward the volatiles associated with the fruit‐ripening process (Keesey et al, 2015).…”

“…Recent studies have focused on finding unique physiological aspects of D. suzukii from ecological and molecular adaptions, that could be good biological targets to develop alternatives to chemical control tools (Hickner et al, 2016; Nguyen et al, 2016; Ramasamy et al, 2016). Behavioral, electrophysiological and bioinformatic approaches have been applied to identify specific plant volatiles and chemosensory genes for D. suzukii (Abraham et al, 2015; Crava et al, 2016; Hickner et al, 2016; Keesey et al, 2015; Ramasamy et al, 2016; Revadi et al, 2015). To date, many antennae‐enriched genes have been identified and characterized to determine their olfactory functions for inter‐ or intra‐specific communications.…”