An invasive whitefly feeding on a virus-infected plant increased its egg production and realized fecundity

Abstract

Background: Plant-pathogenic begomoviruses have a complex association with their insect vectors. The interactions of begomoviruses and reproduction of their vectors are poorly understood. Bemisia tabaci is known to transmit many begomoviruses, and the spread of B. tabaci, especially the B and Q 'biotypes', has been accompanied by the epidemics of begomoviruses. One of these identified disease-causing agents was Tomato yellow leaf curl China virus (TYLCCNV).

Methodology/principal findings: In this study, we compared the egg production and realized fecundity of two 'biotypes' or putative species of the whitefly B. tabaci, including the alien invasive B and the indigenous ZHJ1 from Zhejiang, China, feeding on either healthy or TYLCCNV-infected tobacco plants. The ovary of the whitefly was composed of 12-22 telotrophic ovarioles. According to the morphology of the oocytes and level of yolk content, oocytes in ovarioles were divided into four developmental phases (I-IV). Significantly higher proportion of immature oocytes (phase II, III) and mature oocytes (phase IV) was observed in ovary of females that fed on TYLCCNV-infected tobacco compared to that on healthy plants. Moreover, there was significant increase of eggs laid of B whitefly that fed on TYLCCNV-infected tobacco plants during the early developmental stages. In contrast, the proportion of oocytes of different developmental phases and eggs laid had no significant differences between ZHJ1 whiteflies feeding on TYLCCNV-infected and non-infected host plants.

Conclusions/significance: The invasive B whitefly benefits from feeding on a begomovirus-infected plant through increased egg production and realized fecundity.

Figure 1. Ovary of B whitefly at different developmental stages after eclosion.

A: the ovary of freshly emerged whitefly; B: 1–2 d after eclosion; C: 3–10 d after eclosion; D: 11–14 d after eclosion. Mature oocytes were showed with white arrows. Bacteriocyte sphere was showed with blank arrows. Scale bar: 0.10 mm.

Figure 2. Oocytes of different developmental phases in the ovarioles of whitefly.

A, B, C and D are termed as phase I, phase II, phase III and phase IV, respectively (showed with white arrows). Bacteriocyte sphere was showed with blank arrows. Scale bar: 0.05 mm.

Figure 3. Proportion of different phase oocytes in the ovary of B whitefly.

A, B, C, D: phase I, II, III, IV. The data are expressed as means ± SE (n = 10). At the same day, values followed by the asterisk (*) represent significant differences (P<0.05, Student t-test).

Figure 4. Proportion of different phase oocytes in the ovary of ZHJ1 whitefly.

A, B, C, D: phase I, II, III, IV. The data are expressed as means ± SE (n = 10).

Figure 5. Total numbers of oocytes in the ovaries of two cryptic B. tabaci.

The data are expressed as means ± SE (n = 10). At the same day, values followed by the asterisk (*) represent significant differences (P<0.05, Student t-test).

Figure 6. Fecundity of non-viruliferous adults fed on healthy or virus-infected tobacco of two cryptic whiteflies in the first 8 d after eclosion.

The data are expressed as means ± SE (n = 10). Values followed by the asterisk (*) represent significant differences (P<0.05, Student t-test).

Figure 7. Total number of eggs plus mature oocytes of non-viruliferous adult fed on healthy or virus-infected tobacco of two cryptic whiteflies in the first 2 d after eclosion.

The data are expressed as means ± SE (n = 80). Values followed by the asterisk (*) represent significant differences (P<0.05, Student t-test).