scholarly journals Behavioral and genomic sensory adaptations underlying the pest activity of Drosophila suzukii

2020 ◽  
Author(s):  
Sylvia M. Durkin ◽  
Mahul Chakraborty ◽  
Antoine Abrieux ◽  
Kyle M. Lewald ◽  
Alice Gadau ◽  
...  

ABSTRACTStudying 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 as compared to 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. Secondly, 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. Lastly, 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.

Author(s):  
Sylvia M Durkin ◽  
Mahul Chakraborty ◽  
Antoine Abrieux ◽  
Kyle M Lewald ◽  
Alice Gadau ◽  
...  

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 as compared to 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. Secondly, 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. Lastly, 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.


Insects ◽  
2019 ◽  
Vol 10 (12) ◽  
pp. 454 ◽  
Author(s):  
Jeroen T. Alkema ◽  
Marcel Dicke ◽  
Bregje Wertheim

Sustainable pest control requires a systems approach, based on a thorough ecological understanding of an agro-ecosystem. Such fundamental understanding provides a basis for developing strategies to manipulate the pest’s behaviour, distribution, and population dynamics, to be employed for crop protection. This review focuses on the fundamental knowledge required for the development of an effective push-pull approach. Push-pull is a strategy to repel a pest from a crop, while attracting it toward an external location. It often relies on infochemicals (e.g., pheromones or allelochemicals) that are relevant in the ecology of the pest insect and can be exploited as lure or repellent. Importantly, responsiveness of insects to infochemicals is dependent on both the insect’s internal physiological state and external environmental conditions. This context-dependency reflects the integration of cues from different sensory modalities, the effect of mating and/or feeding status, as well as diurnal or seasonal rhythms. Furthermore, when the costs of responding to an infochemical outweigh the benefits, resistance can rapidly evolve. Here, we argue that profound knowledge on context-dependence is important for the development and implementation of push-pull approaches. We illustrate this by discussing the relevant fundamental knowledge on the invasive pest species Drosophila suzukii as an example.


2020 ◽  
Vol 152 (4) ◽  
pp. 490-515 ◽  
Author(s):  
Yvonne Young ◽  
Tristan A.F. Long

AbstractThe characteristics of the juvenile developmental environment of an individual can have many important consequences for their adult reproductive success as it may shape the development and expression of phenotypes that are relevant to the later operation of sexual selection. Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) is an economically important invasive pest species that lays its eggs in many types of soft fruits and potentially experiences large intrapopulation spatial and temporal variation in its nutritional developmental environments. Here, we examine whether the larval nutritional developmental environment influences D. suzukii mate choice, egg production, and offspring performance. Using D. suzukii raised on diets differing in their nutritional quality, we examined mating preferences, fecundity, and offspring survivorship in “no-choice,” “female choice,” and “male choice” reproductive contexts. We found evidence for both adaptive and nonadaptive mate choice behaviours associated with the phenotypes of D. suzukii that had developed in different nutritional environments. These results reveal the complex nature of the relationship between the developmental environment and individual reproductive success in D. suzukii, which has important potential implications for future management plans involving this species.


2019 ◽  
Author(s):  
Cristina Maria Crava ◽  
Roberto Romani ◽  
Damiano Zanini ◽  
Simone Amati ◽  
Giorgia Sollai ◽  
...  

ABSTRACTDrosophila suzukii is an invasive agricultural pest species that lays eggs in fruit during ripening, while most closely related Drosophila species use rotten matter as oviposition substrates. This behaviour is allowed by an enlarged and serrated ovipositor that can pierce intact fruit skin. D. suzukii combines multiple sensory systems (mechanosensation, olfaction, and taste) to select oviposition sites. Here, we test the hypothesis that the D. suzukii ovipositor is involved in these sensory modalities. We first investigate the ovipositor gene expression using a comparative framework of four Drosophila species with gradual changes in ovipositor morphology to identify evolutionary adaptations specific to D. suzukii. Results show transcription of chemoreceptors and mechanoreceptors in the four species, with a common core of sensory receptors expressed in all of them. Then, we demonstrate that sensory structures present in the distal tip of the D. suzukii ovipositor are mechanosensory-like sensilla, and that the degenerin/epithelial sodium channel ppk is expressed in homologous structures in Drosophila melanogaster. Our results suggest the D. suzukii ovipositor playing a role in mechanosensation, which might be shared with other Drosophila species.


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Hany KM Dweck ◽  
Gaëlle JS Talross ◽  
Wanyue Wang ◽  
John R Carlson

Although most Drosophila species lay eggs in overripe fruit, the agricultural pest Drosophila suzukii lays eggs in ripe fruit. We found that changes in bitter taste perception have accompanied this adaptation. We show that bitter-sensing mutants of Drosophila melanogaster undergo a shift in egg laying preference toward ripe fruit. D. suzukii has lost 20% of the bitter-sensing sensilla from the labellum, the major taste organ of the head. Physiological responses to various bitter compounds are lost. Responses to strawberry purées are lost from two classes of taste sensilla. Egg laying is not deterred by bitter compounds that deter other species. Profiling of labellar transcriptomes reveals reduced expression of several bitter Gr genes (gustatory receptors). These findings support a model in which bitter compounds in early ripening stages deter egg laying in most Drosophila species, but a loss of bitter response contributes to the adaptation of D. suzukii to ripe fruit.


2015 ◽  
Vol 282 (1804) ◽  
pp. 20143018 ◽  
Author(s):  
Teun Dekker ◽  
Santosh Revadi ◽  
Suzan Mansourian ◽  
Sukanya Ramasamy ◽  
Sebastien Lebreton ◽  
...  

The Drosophila pheromone cis -11-octadecenyl acetate ( c VA) is used as pheromone throughout the melanogaster group and fulfils a primary role in sexual and social behaviours. Here, we found that Drosophila suzukii , an invasive pest that oviposits in undamaged ripe fruit, does not produce c VA. In fact, its production site, the ejaculatory bulb, is atrophied. Despite loss of c VA production, its receptor, Or67d, and cognate sensillum, T1, which are essential in c VA-mediated behaviours, were fully functional. However, T1 expression was dramatically reduced in D. suzukii , and the corresponding antennal lobe glomerulus, DA1, minute. Behavioural responses to c VA depend on the input balance of Or67d neurons (driving c VA-mediated behaviours) and Or65a neurons (inhibiting c VA-mediated behaviours). Accordingly, the shifted input balance in D. suzukii has reversed c VA's role in sexual behaviour: perfuming D. suzukii males with Drosophila melanogaster equivalents of c VA strongly reduced mating rates. c VA has thus evolved from a generic sex pheromone to a heterospecific signal that disrupts mating in D. suzukii , a saltational shift, mediated through offsetting the input balance that is highly conserved in congeneric species. This study underlines that dramatic changes in a species' sensory preference can result from rather ‘simple’ numerical shifts in underlying neural circuits.


Insects ◽  
2021 ◽  
Vol 12 (10) ◽  
pp. 923
Author(s):  
Katerina Nikolouli ◽  
Fabiana Sassù ◽  
Spyridon Ntougias ◽  
Christian Stauffer ◽  
Carlos Cáceres ◽  
...  

The Spotted-Wing Drosophila fly, Drosophila suzukii, is an invasive pest species infesting major agricultural soft fruits. Drosophila suzukii management is currently based on insecticide applications that bear major concerns regarding their efficiency, safety and environmental sustainability. The sterile insect technique (SIT) is an efficient and friendly to the environment pest control method that has been suggested for the D. suzukii population control. Successful SIT applications require mass-rearing of the strain to produce competitive and of high biological quality males that will be sterilized and consequently released in the wild. Recent studies have suggested that insect gut symbionts can be used as a protein source for Ceratitis capitata larval diet and replace the expensive brewer’s yeast. In this study, we exploited Enterobacter sp. AA26 as partial and full replacement of inactive brewer’s yeast in the D. suzukii larval diet and assessed several fitness parameters. Enterobacter sp. AA26 dry biomass proved to be an inadequate nutritional source in the absence of brewer’s yeast and resulted in significant decrease in pupal weight, survival under food and water starvation, fecundity, and adult recovery.


Author(s):  
Johanna Elsensohn ◽  
Hannah Burrack

1. Context and need for work The effects and extent of the impacts of agricultural insect pests in and around cropping systems is a rich field of study. However, little research exists on the presence and consequence of pest insects in undisturbed landscapes distant from crop hosts. Research in such areas may yield novel or key insights on pest behavior or ecology that is not evident from agroecosystem-based studies. 2. Approach and methods Using the invasive fruit pest Drosophila suzukii (Matsumura) as a case study, we investigated the presence and resource use patterns of this agricultural pest in wild blackberries growing within the southern Appalachian Mountain range of North Carolina over two years. 3. Main results We found D. suzukii throughout the sampled range with higher levels of infestation (D. suzukii eggs/g fruit) in all ripeness stages in natural areas as compared to cultivated blackberry samples, but especially in under-ripe fruit. 4. Main results We also explored a direct comparison of oviposition preference between wild and cultivated fruit and found higher oviposition in wild berries when equal weights of fruit were offered, but oviposition was higher in cultivated berries when fruit number was equal. 5. Synthesis and applications D. suzukii were wide-spread in previously unsampled remote, forest habitats. Forest populations laid more eggs in unripe wild-grown blackberries throughout the year than populations infesting cultivated berries. This suggests D. suzukii may change its oviposition and foraging behavior in relation to fruit type. Additionally, as D. suzukii exploits a common forest fruit prior to ripeness, further research is needed to explore how this affects wild food web dynamics and spillover to regional agroecosystems.


Author(s):  
Sarah Petermann ◽  
Sabine Otto ◽  
Gerrit Eichner ◽  
Marc F. Schetelig

AbstractNative to Southeast Asia, the spotted wing drosophila (SWD), Drosophila suzukii Matsumura, rapidly invaded America and Europe in the past 20 years. As a crop pest of soft-skinned fruits with a wide range of host plants, it threatens the fruit industry worldwide, causing enormous economic losses. To control this invasive pest species, an understanding of its population dynamics and structure is necessary. Here, we report the population genetics and development of SWD in Germany from 2017–19 using microsatellite markers over 11 different sample sites. It is the first study that examines SWD’s genetic changes over 3 years compared to multiple international SWD laboratory strains. Results show that SWD populations in Germany are highly homogenous without differences between populations or years, which indicates that populations are well adapted, migrate freely, and multiple invasions from outside Germany either did not take place or are negligible. Such high genetic variability and migration between populations could allow for a fast establishment of the pest species. This is especially problematic with regard to the ongoing spread of this invasive species and could bear a potential for developing pesticide resistance, which could increase the impact of the SWD further in the future.


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