The making of a pest: Insights from the evolution of chemosensory receptor families in a pestiferous and invasive fly, Drosophila suzukii

Hickner, Paul V.; Rivaldi, Chissa L.; Johnson, Cole M.; Siddappaji, Madhura H.; Raster, Gregory J.; Syed, Zainulabeuddin

doi:10.1186/s12864-016-2983-9

Cited by 48 publications

(54 citation statements)

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“…We propose that the evolutionary origin of D. suzukii as a pest species was therefore made possible by the progressive tuning of multiple sensory systems, which might be mirrored in changes in its sensory receptor genes [28, 29] or the determinants of neuronal connectivity. Our results suggest that these traits may have emerged in a clade predisposed [26] for this behavioral shift.…”

Section: Resultsmentioning

confidence: 99%

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

et al. 2017

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SummaryThe rise of a pest species represents a unique opportunity to address how species evolve new behaviors and adapt to novel ecological niches [1]. 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 [2]. 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 [3, 4, 5, 6, 7, 8]. D. suzukii has evolved an enlarged, serrated ovipositor that presumably plays a key role by enabling females to pierce the skin of ripe fruit [9]. 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.

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Section: Resultsmentioning

confidence: 99%

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

et al. 2017

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“…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.…”

Section: Methodsmentioning

confidence: 99%

“…Similar molecules involved in these biological signals have also been found and characterized from other fly species, including Drosophila suzukii . However, recent studies on D. suzukii indicate the fly evolved strategically to become well adapted to a unique ecological niche using their specific olfactory system related to feeding and egg‐laying behaviors (Hickner et al, 2016; Karageorgi et al, 2017; Keesey, Knaden, & Hansson, 2015; Ramasamy et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

“…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).…”

Section: Introductionmentioning

confidence: 99%

“…Although chemical insecticides are effective, they have negative impacts on the environment and human health, less likely representing a sustainable pest management strategy. 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).…”

Section: Introductionmentioning

confidence: 99%

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Sex‐biased gene expression in antennae of Drosophila suzukii

Ahn

Corcoran

et al. 2020

Arch Insect Biochem Physiol

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Drosophila suzukii differs from other members of the genus Drosophila in its host preference and oviposition behavior. The flies are attracted to ripening fruits, and females have a serrated ovipositor enabling eggs to be laid inside the fruit. In addition to its huge economic impact, its unique chemoecological, morphological, and physiological characteristics have garnered considerable research interests. In this study, we analyzed D. suzukii antennal transcriptomes to identify sex‐biased genes by comparison of differential gene expressions between male antennae (MA) and female antennae (FA). Among 13,583 total genes of the fly genome, 11,787 genes were expressed in either MA or FA. There are only 132 genes (9 in MA, 7 in FA, and 116 in both, FPKM >1) were expressed in antennae exclusively, and 2,570 genes (9 in MA, 0 in FA, and 2,561 in both) were enriched in antennae containing 185 and 113 sex‐biased genes in MA and FA, respectively. Interestingly, many immune‐related genes were highly expressed in MA, whereas several chemosensory genes were at high rank in FA. We identified 27 sex‐biased chemosensory genes including odorant and gustatory receptors, odorant‐binding proteins, chemosensory proteins, ionotropic receptors, and cytochrome P450s, and validated the gene expressions using quantitative real‐time PCR. The highly expressed sex‐biased genes in antennae are likely involved in the fly specific mating, host‐finding behaviors, or sex‐specific functions. The molecular results demonstrated here will facilitate to find the unique chemoreception of D. suzukii, as well as on the development of new management strategies for this pest.

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Enormous expansion of the chemosensory gene repertoire in the omnivorous German cockroach Blattella germanica

et al. 2018

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The acquisition of genome sequences from a wide range of insects and other arthropods has revealed a broad positive correlation between the complexity of their chemical ecology and the size of their chemosensory gene repertoire. The German cockroach Blattella germanica is an extreme omnivore and has the largest chemosensory gene repertoire known for an arthropod, exceeding even the highly polyphagous spider mite Tetranychus urticae. While the Odorant Receptor family is not particularly large, with 123 genes potentially encoding 134 receptors (105 intact), the Gustatory Receptor family is greatly expanded to 431 genes potentially encoding 545 receptors (483 intact), the largest known for insects and second only to the spider mite. The Ionotropic Receptor family of olfactory and gustatory receptors is vastly expanded to at least 897 genes (604 intact), the largest size known in arthropods, far surpassing the 150 known from the dampwood termite Zootermopsis nevadensis. Commensurately, the Odorant Binding Protein family is expanded to the largest known for insects at 109 genes (all intact). Comparison with the far more specialized, but phylogenetically related termite, within the Dictyoptera, reveals considerable gene losses from the termite, and massive species‐specific gene expansions in the cockroach. The cockroach has lost function of 11%–41% of these three chemoreceptor gene families to pseudogenization, and most of these are young events, implying rapid turnover of genes along with these major expansions, presumably in response to changes in its chemical ecology.

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The making of a pest: Insights from the evolution of chemosensory receptor families in a pestiferous and invasive fly, Drosophila suzukii

Cited by 48 publications

References 100 publications

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

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

Sex‐biased gene expression in antennae of Drosophila suzukii

Enormous expansion of the chemosensory gene repertoire in the omnivorous German cockroach Blattella germanica

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