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Linking genomics and ecology to investigate the complex evolution of an invasive Drosophila pest.

ABSTRACT: Drosophilid fruit flies have provided science with striking cases of behavioral adaptation and genetic innovation. A recent example is the invasive pest Drosophila suzukii, which, unlike most other Drosophila, lays eggs and feeds on undamaged, ripening fruits. This not only poses a serious threat for fruit cultivation but also offers an interesting model to study evolution of behavioral innovation. We developed genome and transcriptome resources for D. suzukii. Coupling analyses of these data with field observations, we propose a hypothesis of the origin of its peculiar ecology. Using nuclear and mitochondrial phylogenetic analyses, we confirm its Asian origin and reveal a surprising sister relationship between the eugracilis and the melanogaster subgroups. Although the D. suzukii genome is comparable in size and repeat content to other Drosophila species, it has the lowest nucleotide substitution rate among the species analyzed in this study. This finding is compatible with the overwintering diapause of D. suzukii, which results in a reduced number of generations per year compared with its sister species. Genome-scale relaxed clock analyses support a late Miocene origin of D. suzukii, concomitant with paleogeological and climatic conditions that suggest an adaptation to temperate montane forests, a hypothesis confirmed by field trapping. We propose a causal link between the ecological adaptations of D. suzukii in its native habitat and its invasive success in Europe and North America.

SUBMITTER: Ometto L

PROVIDER: S-EPMC3641628 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Linking genomics and ecology to investigate the complex evolution of an invasive Drosophila pest.

Ometto Lino L Cestaro Alessandro A Ramasamy Sukanya S Grassi Alberto A Revadi Santosh S Siozios Stefanos S Moretto Marco M Fontana Paolo P Varotto Claudio C Pisani Davide D Dekker Teun T Wrobel Nicola N Viola Roberto R Pertot Ilaria I Cavalieri Duccio D Blaxter Mark M Anfora Gianfranco G Rota-Stabelli Omar O

Genome biology and evolution 20130101 4

Drosophilid fruit flies have provided science with striking cases of behavioral adaptation and genetic innovation. A recent example is the invasive pest Drosophila suzukii, which, unlike most other Drosophila, lays eggs and feeds on undamaged, ripening fruits. This not only poses a serious threat for fruit cultivation but also offers an interesting model to study evolution of behavioral innovation. We developed genome and transcriptome resources for D. suzukii. Coupling analyses of these data wi ...[more]

PMID: 23501831

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Project description:BackgroundDrosophila suzukii differs from other melanogaster group members in their proclivity for laying eggs in fresh fruit rather than in fermenting fruits. Olfaction and gustation play a critical role during insect niche formation, and these senses are largely mediated by two important receptor families: olfactory and gustatory receptors (Ors and Grs). Earlier work from our laboratory has revealed how the olfactory landscape of D. suzukii is dominated by volatiles derived from its unique niche. Signaling and reception evolve in synchrony, since the interaction of ligands and receptors together mediate the chemosensory behavior. Here, we manually annotated the Ors and Grs in D. suzukii and two close relatives, D. biarmipes and D. takahashii, and compared these repertoires to those in other melanogaster group drosophilids to identify candidate chemoreceptors associated with D. suzukii's unusual niche utilization.ResultsOur comprehensive annotations of the chemosensory genomes in three species, and comparative analysis with other melanogaster group members provide insights into the evolution of chemosensation in the pestiferous D. suzukii. We annotated a total of 71 Or genes in D. suzukii, with nine of those being pseudogenes (12.7 %). Alternative splicing of two genes brings the total to 62 genes encoding 66 Ors. Duplications of Or23a and Or67a expanded D. suzukii's Or repertoire, while pseudogenization of Or74a, Or85a, and Or98b reduced the number of functional Ors to roughly the same as other annotated species in the melanogaster group. Seventy-one intact Gr genes and three pseudogenes were annotated in D. suzukii. Alternative splicing in three genes brings the total number of Grs to 81. We identified signatures of positive selection in two Ors and three Grs at nodes leading to D. suzukii, while three copies in the largest expanded Or lineage, Or67a, also showed signs of positive selection at the external nodes.ConclusionOur analysis of D. suzukii's chemoreceptor repertoires in the context of nine melanogaster group drosophilids, including two of its closest relatives (D. biarmipes and D. takahashii), revealed several candidate receptors associated with the adaptation of D. suzukii to its unique ecological niche.

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.

Dataset Information

Linking genomics and ecology to investigate the complex evolution of an invasive Drosophila pest.

Publications

Linking genomics and ecology to investigate the complex evolution of an invasive Drosophila pest.

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