Resource use by individual Drosophila suzukii reveals a flexible preference for oviposition into healthy fruits

Abstract

The invasive pest fruit fly Drosophila suzukii is thought to be a specialist on healthy, i.e. unwounded, non-fermenting fruits. Morphological (sharp ovipositor) and neurophysiological/behavioural adaptations have been suggested to contribute to distinct adult feeding (wounded/microbe-laden fruits) and reproductive (healthy fruits) sites. We tested whether (1) variation in the overall availability of fruits, (2) variation in fruit type (healthy, wounded, fermenting), and (3) the relative abundance of different fruit types are ecological determinants of D. suzukii egg-laying decisions. even though individual flies reduced their reproductive output when resource availability (blueberries) was low, a significantly higher proportion of eggs was allocated to healthy fruits, relative to wounded and fermenting fruits. However, the preference for healthy over wounded fruits declined continuously with a decrease in the relative abundance of healthy fruits and the overall reproductive output did not change. Under laboratory conditions, D. suzukii larvae achieved a higher developmental success on wounded than on healthy blueberries, but suffered less from density-dependent competition in healthy fruits. these data suggest that D. suzukii, despite showing an egg-laying preference for healthy fruits, also uses wounded/fermenting fruits as egg-laying sites, and that it may thrive well in windfall fruits.Drosophila suzukii, a devastating invasive insect in European and American fruit plantations, has been described as being '…extremely fond of otherwise undamaged, ripening fruits…' 1 . Indeed, unlike most other drosophilid fruit fly species that are able to use only fruits with cracked skins for egg-laying, a serrated ovipositor enables D. suzukii to pierce the intact skin of many cultured and wild fruits and to insert their eggs into the fresh fruit flesh 2 . The subsequent larval development and microbial growth cause a rapid fruit decay that renders cherries, blue-, straw-, and blackberries etc. unmarketable. Recently, Karageorgi et al. 3 showed that an egg-laying preference of D. suzukii for intact ripening over rotting strawberries is mediated by a combination of chemo-and mechanosensation. This apparent preference has been suggested to have resulted in distinct adult feeding and breeding sites 4 . Studies designed for describing neurophysiologically 'hard-wired' preferences, however, often overlook the impact of variation in experience and internal status, i.e. optimal foraging decisions 5 , as well as neural limitations in detecting the preferred host in naturally complex ecological settings 6 .Conclusions regarding such 'hard-wired' preferences are particularly problematic for polyphagous insects 7like D. suzukii -where individuals are confronted with hosts that vary widely in suitability and availability. For example, the extent to which a particular host is used for oviposition may be affected by the type and density of alternative hosts in the vicinity, resulting in apparently suboptimal host use 8 . Suboptimal host u...

Drosophila suzukiiavoidance of microbes in oviposition choice

“…Karageorgi et al . [ 6 ] showed that when given the choice between ripe and rotten strawberry fruits, D. suzukii strongly preferred ripe over rotten fruit, whereas Drosophila melanogaster showed an opposite tendency and preferred rotten fruit, consistent with other studies [ 7 , 8 ]. In the same experiment, Drosophila biarmipes , a closely related species of D. suzukii showed no preference between ripe and rotten fruit, indicating that they are at an intermediate evolutionary stage between D. suzukii and D. melanogaster .…”

“…Assessing the fruit condition and making the decision to select the oviposition site involve an integration of multiple sensory cues. It has been shown that D. suzukii has the ability to make complex decisions between healthy and fermenting fruits depending on the availability of the resource [ 8 ]. We hypothesize that one of the unexplored factors that D. suzukii sense could be the commensal microbes on fermenting fruits that have been deposited by conspecific and heterospecific individuals.…”

Drosophila suzukiiavoidance of microbes in oviposition choice

“…In late fruiting season when the majority of the fruits are on the ground and rotten, the females may readily lay eggs onto suboptimal fermenting fruits, the situation resembling our assays using only inoculated substrates (figure 3). These explanations are consistent with the study by Kienzle et al [8], which showed that D. suzukii exhibit stronger preferences toward ovipositing in healthy fruits when healthy and fermenting fruits are both abundant compared to when the former are less abundant. The context dependent optimization through seasonal change in host fruit condition might explain the evolutionary background of our findings where substrate hardness takes precedence over microbial presence in the decision to oviposit in this species.…”

“…Karageorgi et al . [6] showed that when given the choice between ripe and rotten strawberry fruits, D. suzukii strongly preferred ripe over rotten fruit, whereas D. melanogaster showed an opposite tendency and preferred rotten fruit, consistent with other studies [7,8]. In the same experiment, D. biarmipes , a closely related species of D. suzukii , showed no preference between ripe and rotten fruit, indicating that they are at an intermediate evolutionary stage between D. suzukii and D. melanogaster .…”

“…Assessing the fruit condition and making the decision to select the oviposition site involve an integration of multiple sensory cues. It has been shown that D. suzukii has the ability to make complex decisions between healthy and fermenting fruits depending on the availability of the resource [8]. In D. melanogaster , mechanosensory (texture) and chemosensory (taste) information are integrated to direct feeding and oviposition decisions [25–27].…”