Preference of Pentalonia nigronervosa for infected banana plants tends to reverse after Banana bunchy top virus acquisition

Abstract

Pentalonia nigronervosa Coquerel (Hemiptera: Aphididae) is the vector of the Banana Bunchy Top Virus (BBTV), the most serious viral disease of banana (Musa spp.) in the world. Before acquiring the virus, the vector is more attracted to infected banana plants in response to the increased emissions of volatile organic compounds (VOCs). Here, we test the hypothesis that BBTV acquisition directly modifies the preference of P. nigronervosa for infected banana plants, and that the change in preference results from the alteration of the organs linked to the VOC detection or to the behaviour of the vector. We found that the preference of P. nigronervosa for infected banana plants reverses after virus acquisition in dessert banana, while it remains similar between healthy and infected banana plants before and after the acquisition of BBTV. At the same time, aphids reared on infected bananas had smaller forewing areas and hind tibia length than aphids reared on healthy bananas, although the number of secondary rhinaria on the antennae was lower on dessert banana-reared aphids than plantain-reared aphids, this was not affected by the infection status of the aphid. These results support the "vector manipulation hypothesis-VMH" of pathogens to promote their spread. They have implications for the BBTV management.

Figure 1

Comparison of the choice of viruliferous and non-viruliferous alate aphids on banana plants. The average number of aphids per plant is shown with standard deviation, (N = 20 replicates, each time with 20 aphids per experiment). NS not significant, (*): p value < 0.05, (***): p value < 0.001. (A) Healthy dessert banana and infected dessert banana, (B) healthy plantain and infected plantain, (C) infected dessert banana and infected plantain, (D) healthy dessert banana and healthy plantain. HDB healthy dessert banana, IDB infected dessert banana, HPB healthy plantain banana, IPB infected plantain banana.

Figure 2

Effect of BBTV on (A) average length of hind tibiae (mm), (B) average forewing area (mm²) and (C) average number of SR on antennae of aphid reared on the four kind of banana plants: HDB healthy dessert banana, IDB infected dessert banana, HPB healthy plantain banana, IPB infected plantain banana. Means with standard errors (N = 20). Statistical results (GLM): NS indicate non-significant results (p > 0.05), stars indicate significant differences (p < 0.05) between infection statuses (for each genotype) and different letters indicate significant differences (p < 0.05) between genotypes (upper case letter for healthy plants and lower case letter for infected plants).

Figure 3

Linear correlation (n = 20) between (A) forewing area and hind tibia length, (B) total number of secondary rhinaria on antennae and hind tibia length of P. nigronervosa alates, collected from HDB healthy dessert banana, IDB infected dessert banana, HPB healthy plantain banana, IPB infected plantain banana. Regression line equation and R² is indicated for each correlation.