Tomato spotted wilt virusmanipulates the reproduction of its insect vector, western flower thrips (Frankliniella occidentalis), to facilitate transmission

Abstract

BACKGROUND: Tomato spotted wilt virus (TSWV), one of the most devastating viruses of ornamental plants and vegetable crops worldwide, is transmitted by the western flower thrips, Frankliniella occidentalis (Pergande), in a persistent-propagative manner. How TSWV manipulates the reproduction of its vector to enhance transmission and whether infection with TSWV changes the mating behaviour of this thrips vector are not fully understood. RESULTS:In this study, we found that TSWV-exposed thrips, in general, had a significantly longer developmental time than did non-exposed individuals. Such an increase was predominantly seen in adults, a stage associated with dispersal and virus transmission. TSWV-exposed F. occidentalis produced substantially more progeny than did non-exposed thrips. Interestingly, most of the increase in progeny came from an increase in males, a sex with a greater dispersal and virus transmission capability. Specifically, the sex ratio of progeny shifted from female biased (2-7:1) to evenly split or male biased. Regarding mating behaviour, compared to virus-free controls, TSWV-exposed F. occidentalis had significantly longer copulation duration, were more active in males, and remated less often in females. CONCLUSION: These combined results suggest that TSWV alters the reproductive behaviour of its insect vector, F. occidentalis, to promote virus transmission. Consequently, a monitoring program capable of earlier detection of the virus and a reduced economic threshold for vector (thrips) control should be in consideration for the long-term, sustainable management of TSWV.

Tomato spotted wilt orthotospovirus shifts sex ratio toward males in the western flower thrips, Frankliniella occidentalis, by down‐regulating a FSCB‐like gene

“…A virus‐free F. occidentalis colony was isolated from an indoor strain that had been kept in our laboratory for nearly 20 years. Thrips were fed with fresh bean pods and were kept in glass jars in a climate chamber at 26 ± 1 °C, with 70% relative humidity and a 16 L:8D photoperiod as described by Wan et al 13 . TSWV isolate TSWV‐YN was maintained on Datura stramonium plants by thrips transmission.…”

“…A total of 26 differentially expressed proteins were up-regulated and 17 were downregulated in the CC category; these were mainly enriched in cellular anatomical entity. In the MF category, 27 differentially expressed proteins were up-regulated, which were mainly enriched in binding (13) and catalytic activity (10). The 49 differentially expressed proteins that were down-regulated in the MF category were mainly enriched in binding (23), structural molecule activity (13), and catalytic activity (10).…”

“…32 We previously reported that TSWV-infected male F. occidentalis mated to uninfected females led to a shift in the sex ratio of offspring toward males. 13 The increase of male individuals among F. occidentalis offspring indicates that females produced more unfertilized eggs, that is, that TSWV could potentially change the sex ratio of offspring by influencing the ability of males to fertilize eggs. However, the mechanism by which TSWV regulates the sex ratio of F. occidentalis progeny remains unclear.…”

“…11 Many studies indicate that TSWV has substantial effects on F. occidentalis biology and behavior, increasing the fecundity and lifespan of F. occidentalis while altering its feeding and oviposition preferences. 1,3,9,[12][13][14] These effects benefit both F. occidentalis and TSWV. Interestingly, Wan et al 13 found that exposure to TSWV altered the sex ratio of F. occidentalis offspring.…”

“…In addition to vectoring TSWV, F. occidentalis is on its own a serious pest of horticultural crops worldwide 11 . Many studies indicate that TSWV has substantial effects on F. occidentalis biology and behavior, increasing the fecundity and lifespan of F. occidentalis while altering its feeding and oviposition preferences 1,3,9,12–14 . These effects benefit both F. occidentalis and TSWV.…”