Adaptation by the Brown Planthopper to Resistant Rice: A Test of Female-Derived Virulence and the Role of Yeast-like Symbionts

Abstract

The adaptation by planthoppers to feed and develop on resistant rice is a challenge for pest management in Asia. We conducted a series of manipulative experiments with the brown planthopper (Nilaparvata lugens (Stål)) on the resistant rice variety IR62 (BPH3/BPH32 genes) to assess behavioral and bionomic changes in planthoppers exhibiting virulence adaptation. We also examined the potential role of yeast-like symbionts (YLS) in virulence adaptation by assessing progeny fitness (survival × reproduction) following controlled matings between virulent males or females and avirulent males or females, and by manipulating YLS densities in progeny through heat treatment. We found virulence-adapted planthoppers developed faster, grew larger, had adults that survived for longer, had female-biased progeny, and produced more eggs than non-selected planthoppers on the resistant variety. However, feeding capacity-as revealed through honeydew composition-remained inefficient on IR62, even after 20+ generations of exposure to the resistant host. Virulence was derived from both the male and female parents; however, females contributed more than males to progeny virulence. We found that YLS are essential for normal planthopper development and densities are highest in virulent nymphs feeding on the resistant host; however, we found only weak evidence that YLS densities contributed more to virulence. Virulence against IR62 in the brown planthopper, therefore, involves a complex of traits that encompass a series of behavioral, physiological, and genetic mechanisms, some of which are determined only by the female parent.

Keywords: BPH3; BPH32; Delphacidae; Heteroptera; Integrated Pest Management; endosymbionts; honeydew; host plant resistance; resistance management; rice breeding.

Figure 1

Study predictions based on the vertical transmission of endosymbionts through the egg and a possible role for YLS in virulence adaptation. If endosymbionts determine virulence, then the progeny of virulent females will also be virulent, irrespective of the male parent (A). If the virulent male parent also determines virulence, then progeny virulence will respond in an additive manner to having one or two virulent parents (B). If virulence is determined by either parent (i.e., in the case of a major resistance gene), then progeny with one or two virulent parents, of either sex, will be virulent (C). Where virulence is female-derived, the role of YLS and other vertically transmitted endosymbionts can be assessed by comparing aposymbiotic and symbiotic planthoppers. Where the relative fitness of progeny with virulent or avirulent female parents is affected by removing endosymbionts (aposymbiotic), then the symbionts play a role in virulence adaptation (D). Where relative fitness patterns are maintained despite planthoppers being aposymbiotic, then the endosymbionts play little role in virulence adaptation (E).

Figure 2

Performance of planthopper nymphs (A–D) and adults (E,F) derived (F1) from controlled mating of virulent and non-virulent parents when feeding on the resistant rice variety IR62. Performance was compared by recording (A) honeydew production, (B) nymph development, (C) proportion of adults that were female, (D) nymph weight, (E) the time to 50% and 100% mortality of adult males, and (F) the time to 50% and 100% mortality of adult females (i.e., longevity). Standard errors are indicated (N = 12). NS = no significant parent effect, *** = highly significant parent effect (p < 0.001). Lowercase letters indicate homogenous groups (Tukey p > 0.05). Data in (A) was ranked, (B,C) arcsine-transformed, and (D) log-transformed before analyses.

Figure 3

(A) Oviposition and (B) population development from adults (F1) produced through controlled mating of virulent and non-virulent parents when feeding on the resistant rice variety IR62. Inset graphs indicate the total number of eggs (A) and total number of nymphs (B) derived from mated pairs. Note that eggs and nymphs are F2 individuals. Standard errors are indicated (N = 12). NS = no significant parent effect, *** = highly significant parent effect (p ≤ 0.001). Lowercase letters indicate homogenous groups (Tukey p > 0.05). Egg and nymph numbers were log-transformed and proportions arcsine-transformed before analyses.

Figure 4

(A) Wet weight of unmated adult females (F1) derived from controlled mating between virulent and avirulent planthoppers with (B) the corresponding final weights of IR62 seedlings after planthopper feeding. (C) The estimated densities of YLS at the end of the experiment are also presented. Gray bars represent symbiotic planthoppers and white bars represent aposymbiotic planthoppers. Standard errors are indicated (N = 12). NS = no significant effect, *** = highly significant effect (p < 0.001). Lowercase letters indicate homogenous groups (Tukey p > 0.05). Data were log-transformed before analyses.