Mind the Wound!-Fruit Injury Ranks Higher than, and Interacts with, Heterospecific Cues for Drosophila suzukii Oviposition

Abstract

Drosophila suzukii is a globally distributed insect that infests many economically important fruit varieties by ovipositing into ripening fruits. The mechanisms underlying host selection, in particular the fly's preference for fresh, intact, and competitor-free fruits, are only partially understood. We hypothesize that D. suzukii females use cues of different fruit properties to rank potential host fruits in a hierarchical manner. We created four naturally occurring fruit (blueberries) categories: (1) intact; (2) artificially wounded; (3) wounded + containing eggs of different Drosophila species; and (4) intact + exposed to D. melanogaster. Individual D. suzukii females were offered several fruits in different two-way combinations of the fruit categories. Females showed a robust oviposition preference for intact vs. wounded + infested fruits, which was even stronger compared to the intact-wounded combination. Females preferred ovipositing into intact vs. intact + exposed blueberries; however, they preferred intact + exposed over wounded blueberries. This implies a hierarchical host preference in D. suzukii, which is determined by heterospecific cues (possibly fecal matter components) and an unknown "wounding factor" of fruits.

Keywords: avoidance; host cues; host selection; preference hierarchy.

Figure 1

Proportion of eggs laid by Drosophila suzukii into fresh and intact blueberries, offered together with fruits that were wounded only or wounded and contained egg-laying cues of different Drosophila species (D. melanogaster, D. simulans, D. subobscura); prior to the use of the blueberries in the choice experiments the heterospecific eggs were removed. Intact and fresh fruits were embedded in a matrix of wounded/infested blueberries (a total of 12 berries) that varied in their relative abundance (x-axis), i.e., 2 intact vs. 10 wounded/infested (0.17), 4/8 (0.33), 6/6 (0.5). For better visibility, the data points are staggered around the corresponding values on the x-axis. The solid and colored lines represent the predicted values from the Logistic GLM. The shaded areas show the standard error of the predicted model. The dashed lines represent the expected proportion of D. suzukii eggs in fresh and intact fruits if the female flies had no preference for either host fruit category and distributed their eggs randomly across the twelve blueberries.

Figure 2

Proportion of eggs laid by Drosophila suzukii into specific target fruit category (y-axis) when combined with a different fruit category (x-axis): (A) target category: intact; different category: wounded; (B) target category: intact; different category: exposed; (C) target category: exposed; different category: wounded; (D) target category: wounded; different category: wounded and exposed. For each replicate, the relative abundance was 0.5 in a matrix of 12 blueberries. The dashed lines represent the expected proportion of D. suzukii eggs in the target fruit category if the female flies had no preference for either category and distributed their eggs randomly across the twelve blueberries. The predicted values ± standard errors from the corresponding GLMs are shown. In all combinations, the flies laid a significantly higher proportion of eggs in the target fruit category than expected under the null hypothesis, i.e., flies do not have any preference: (A) t = 3.37, p = 0.003; (B) t = 6.53, p < 0.001; (C) t = 3.87, p < 0.001; (D) t = 2.33, p = 0.030.

Figure 3

Host fruit selection hierarchy in Drosophila suzukii on blueberries. The proportion of eggs laid into different potential host fruit categories revealed an oviposition preference for intact fruits (I) over intact ones carrying cues, probably fecal material, of heterospecific flies (II), followed by wounded fruits (III) and those that were wounded and had heterospecific marks (IV).