The Protein Paradox: Elucidating the Complex Nutritional Ecology of the Invasive Berry Pest, Spotted-Wing Drosophila (Diptera: Drosophila suzukii)

Abstract

Spotted-wing drosophila (SWD), Drosophila suzukii, has become one of the most widely studied insect species over the last decade, largely due to its recent invasion and rapid expansion across the Americas and Europe. Unlike other drosophilid species, which colonize rotting fruit, SWD females possess a serrated ovipositor that allows them to lay eggs in intact ripening fruit, causing significant economic problems for fruit/berry producers worldwide. Though an impressive amount of research has been conducted on SWD's ecology and physiology, aspects of their nutritional ecology remain ambiguous. This review synthesizes the research to date to provide a more comprehensive view of SWD's nutritional relationship with its fruit hosts and associated microbes. Overall, data suggest that SWD's ability to utilize novel resources is likely due to changes in their ecological, rather than physiological, niche that are largely mediated by microbial associations. Studies show that SWD's nutrient intake is comparable to other drosophilid species, indicating limited adaptation to feeding on lower-protein resources. Instead, data show that fruit protein content is a reliable predictor of host suitability and that fruit-microbe dynamics have a strong impact on protein availability. In particularly, fruit protein increases after infestation with SWD-associated microbes, suggesting that initially-suboptimal intact fruits can become protein-rich on a timeframe that is relevant for larval nutrition. This body of work suggests that microbial associations between flies and their fruit hosts can compensate for the nutritional differences between intact and rotting fruit, and that these relationships are likely responsible for SWD's expanded nutritional niche.

Hormetic and transgenerational effects in spotted-wing Drosophila (Diptera: Drosophilidae) in response to three commonly-used insecticides

“…Reductions in efficacy may be due to resistance, which has been detected for some chemistries in California [ 13 ], Michigan [ 14 ], and Georgia [ 15 ]. However, other factors, such as weather [ 12 , 16 ], timing of application [ 12 , 17 – 19 ], pesticide volatilization/degradation [ 20 – 22 ], and penetration into cultivars with high structural complexity [ 23 ], plant nutrient content [ 24 – 26 ], and insecticide resistance [ 14 , 27 , 28 ], can also reduce insecticide efficacy. This can occur by impeding contact between the insecticide and spotted-wing Drosophila adults, considering that spotted-wing Drosophila are small, highly mobile, crepuscular insects that are documented to exhibit daily movement patterns [ 29 – 33 ].…”

Propensity for resistance development in the invasive berry pest, spotted‐wing drosophila (Drosophila suzukii), under laboratory selection

“…These could be genes associated with detoxification, cellular repair, cuticular integrity, or general movement patterns. It is also possible that the laboratory environment, particularly the switch to artificial diet with antimicrobial components, could have impacted the microbiome of the flies in ways that indirectly affected susceptibility 28–31 . For instance, microbial associations have been found to impact insecticide detoxification and resistance in other insect species 32–34 .…”

“…It is also possible that the laboratory environment, particularly the switch to artificial diet with antimicrobial components, could have impacted the microbiome of the flies in ways that indirectly affected susceptibility. 28 , 29 , 30 , 31 For instance, microbial associations have been found to impact insecticide detoxification and resistance in other insect species. 32 , 33 , 34 Differences in microbiome communities have even been documented in laboratory fly colonies that were fed the same diets for over 50 generations, suggesting that other non‐nutritional factors can also affect microbial community structure within laboratory cultures.…”

Effect of acetic acid bacteria colonization on oviposition and feeding site choice inDrosophila suzukiiand its related species

“…However, considering that D. suzukii larvae have limited physiological adaptation to a low-protein diet and intact healthy fruits have seasonally restricted availability, the competitive advantage of ovipositing in ripening fruits can be conditional (Silva-Soares et al, 2017; Young et al, 2018; Kienzle et al, 2020; Deans and Hutchingson 2021). Therefore, the oviposition site preference towards non-fermenting fruits may depend on multiple factors, therefore, there is likely to be variability maintained within species.…”