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Behavioral and Genomic Sensory Adaptations Underlying the Pest Activity of Drosophila suzukii.

ABSTRACT: Studying how novel phenotypes originate and evolve is fundamental to the field of evolutionary biology as it allows us to understand how organismal diversity is generated and maintained. However, determining the basis of novel phenotypes is challenging as it involves orchestrated changes at multiple biological levels. Here, we aim to overcome this challenge by using a comparative species framework combining behavioral, gene expression, and genomic analyses to understand the evolutionary novel egg-laying substrate-choice behavior of the invasive pest species Drosophila suzukii. First, we used egg-laying behavioral assays to understand the evolution of ripe fruit oviposition preference in D. suzukii compared with closely related species D. subpulchrella and D. biarmipes as well as D. melanogaster. We show that D. subpulchrella and D. biarmipes lay eggs on both ripe and rotten fruits, suggesting that the transition to ripe fruit preference was gradual. Second, using two-choice oviposition assays, we studied how D. suzukii, D. subpulchrella, D. biarmipes, and D. melanogaster differentially process key sensory cues distinguishing ripe from rotten fruit during egg-laying. We found that D. suzukii's preference for ripe fruit is in part mediated through a species-specific preference for stiff substrates. Last, we sequenced and annotated a high-quality genome for D. subpulchrella. Using comparative genomic approaches, we identified candidate genes involved in D. suzukii's ability to seek out and target ripe fruits. Our results provide detail to the stepwise evolution of pest activity in D. suzukii, indicating important cues used by this species when finding a host, and the molecular mechanisms potentially underlying their adaptation to a new ecological niche.

SUBMITTER: Durkin SM

PROVIDER: S-EPMC8136512 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Spotted wing drosophila, Drosophila suzukii Matsumura, is a major pest of small fruit worldwide in temperate and subtropical growing regions. In Northern climates, D. suzukii likely overwinters locally under leaf litter and snow pack, but our understanding of the factors affecting thermal susceptibility is limited. While previous investigations of thermal susceptibility in this species have employed conventional static acclimation protocols, we aimed to determine whether gradual cooling, or dynamic acclimation, may extend the limits of known thermal tolerance by more closely approximating naturally occurring shifts in temperature. First, we assessed survival among adult and pupal D. suzukii using static acclimation. Then, we re-assessed survival using a novel dynamic acclimation method. We found that while static acclimation was sufficient to induce cold tolerance, dynamic acclimation significantly improved survival at temperatures as low as -7.5 °C. Following static acclimation, the lower lethal limit of adult D. suzukii was -1.1 °C in winter morphotype (WM) adults compared to 1.7 °C in non-acclimated summer morphotype (SM) adults. Dynamic acclimation reduced the lower limit to -5 °C in SM flies. At the end of our study 50% of WM flies survived 72 h at -7.5 °C. Below 0 °C pupal survival declined significantly regardless of acclimation procedure. However, pupal acclimation improved survival outcomes significantly compared to non-acclimated pupae, suggesting that while juvenile diapause is unlikely, cold hardening likely benefits those flies which may develop into the overwintering WM population. These data suggest that the degree of cold hardening is proportional to the thermal environment, a finding previously unrecognized in this species. Given the economic impact of this pest, these data may have important implications for offseason population monitoring and management. We discuss how phenotypic plasticity may drive geographical range expansion, and the impact of climate change on the spread of this species.

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Behavioral and Genomic Sensory Adaptations Underlying the Pest Activity of Drosophila suzukii.

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