Tomato spotted wilt orthotospovirus influences the reproduction of its insect vector, western flower thrips, Frankliniella occidentalis, to facilitate transmission

Yanran Wan; Sabir Hussain; Austin Merchant; Baoyun Xu; Wen Xie; Shaoli Wang; Youjun Zhang; Xuguo Zhou; Qingjun Wu

doi:10.1002/ps.5779

Tomato spotted wilt orthotospovirus influences the reproduction of its insect vector, western flower thrips, Frankliniella occidentalis, to facilitate transmission

Yanran Wan, Sabir Hussain, Austin Merchant, Baoyun Xu, Wen Xie, Shaoli Wang, Youjun Zhang, Xuguo Zhou, Qingjun Wu

Entomology

Research output: Contribution to journal › Article › peer-review

16 Scopus citations

Abstract

BACKGROUND: Tomato spotted wilt orthotospovirus (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 influences the reproduction of its vector to enhance transmission and whether infection with TSWV changes the mating behavior of F. occidentalis are not fully understood. RESULTS: TSWV-exposed thrips had a significantly longer developmental time than non-exposed individuals. More importantly, increased developmental time was predominantly associated with adults, a stage critical for dispersal and virus transmission. In addition, 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 female/male ratio of progeny shifted from 1.3–7.0/1 to 0.6–1.1/1. As for mating behavior, copulation time was significantly longer in TSWV-exposed thrips. Finally, females tended to re-mate less when exposed to the virus. Resistance to re-mating may lead to reduced sperm availability in females, which translates to a larger number of male progeny under a haplodiploid system. CONCLUSION: These combined results suggest that TSWV can influence the developmental time, mating behavior, fecundity, and offspring sex allocation of its vector F. occidentalis to facilitate virus transmission. As such, a monitoring program capable of the earlier detection of the virus in host plants and/or its insect vector, thrips, using double-antibody sandwich enzyme-linked immunosorbent assay (DAS-ELISA), real time quantitative polymerase chain reaction (RT-qPCR) or virus detection strips might be beneficial for long-term, sustainable management.

Original language	English
Pages (from-to)	2406-2414
Number of pages	9
Journal	Pest Management Science
Volume	76
Issue number	7
DOIs	https://doi.org/10.1002/ps.5779
State	Published - Jul 1 2020

Bibliographical note

Funding Information:
This study was funded by the National Key R&D Program of China (2017YFD0201000), the Natural Science Foundation of China (31772199, 31572037), the Science and Technology Innovation Program of the CAAS (AAS-ASTIP-IVFCAAS), the Beijing Leafy Vegetables Innovation Team of the Modern Agro-industry Technology Research System (BAIC07-2018), and the Beijing Key Laboratory for Pest Control and Sustainable Cultivation of Vegetables.

Publisher Copyright:
© 2020 Society of Chemical Industry

Keywords

Frankliniella occidentalis
development
mating behavior
sex ratio allocation
tomato spotted wilt orthotospovirus

ASJC Scopus subject areas

Agronomy and Crop Science
Insect Science

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10.1002/ps.5779

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@article{a360f9ab436a44b09eca669b74d29f2b,

title = "Tomato spotted wilt orthotospovirus influences the reproduction of its insect vector, western flower thrips, Frankliniella occidentalis, to facilitate transmission",

abstract = "BACKGROUND: Tomato spotted wilt orthotospovirus (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 influences the reproduction of its vector to enhance transmission and whether infection with TSWV changes the mating behavior of F. occidentalis are not fully understood. RESULTS: TSWV-exposed thrips had a significantly longer developmental time than non-exposed individuals. More importantly, increased developmental time was predominantly associated with adults, a stage critical for dispersal and virus transmission. In addition, 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 female/male ratio of progeny shifted from 1.3–7.0/1 to 0.6–1.1/1. As for mating behavior, copulation time was significantly longer in TSWV-exposed thrips. Finally, females tended to re-mate less when exposed to the virus. Resistance to re-mating may lead to reduced sperm availability in females, which translates to a larger number of male progeny under a haplodiploid system. CONCLUSION: These combined results suggest that TSWV can influence the developmental time, mating behavior, fecundity, and offspring sex allocation of its vector F. occidentalis to facilitate virus transmission. As such, a monitoring program capable of the earlier detection of the virus in host plants and/or its insect vector, thrips, using double-antibody sandwich enzyme-linked immunosorbent assay (DAS-ELISA), real time quantitative polymerase chain reaction (RT-qPCR) or virus detection strips might be beneficial for long-term, sustainable management.",

keywords = "Frankliniella occidentalis, development, mating behavior, sex ratio allocation, tomato spotted wilt orthotospovirus",

author = "Yanran Wan and Sabir Hussain and Austin Merchant and Baoyun Xu and Wen Xie and Shaoli Wang and Youjun Zhang and Xuguo Zhou and Qingjun Wu",

note = "Funding Information: This study was funded by the National Key R&D Program of China (2017YFD0201000), the Natural Science Foundation of China (31772199, 31572037), the Science and Technology Innovation Program of the CAAS (AAS-ASTIP-IVFCAAS), the Beijing Leafy Vegetables Innovation Team of the Modern Agro-industry Technology Research System (BAIC07-2018), and the Beijing Key Laboratory for Pest Control and Sustainable Cultivation of Vegetables. Publisher Copyright: {\textcopyright} 2020 Society of Chemical Industry",

year = "2020",

month = jul,

day = "1",

doi = "10.1002/ps.5779",

language = "English",

volume = "76",

pages = "2406--2414",

number = "7",

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T1 - Tomato spotted wilt orthotospovirus influences the reproduction of its insect vector, western flower thrips, Frankliniella occidentalis, to facilitate transmission

AU - Wan, Yanran

AU - Hussain, Sabir

AU - Merchant, Austin

AU - Xu, Baoyun

AU - Xie, Wen

AU - Wang, Shaoli

AU - Zhang, Youjun

AU - Zhou, Xuguo

AU - Wu, Qingjun

N1 - Funding Information: This study was funded by the National Key R&D Program of China (2017YFD0201000), the Natural Science Foundation of China (31772199, 31572037), the Science and Technology Innovation Program of the CAAS (AAS-ASTIP-IVFCAAS), the Beijing Leafy Vegetables Innovation Team of the Modern Agro-industry Technology Research System (BAIC07-2018), and the Beijing Key Laboratory for Pest Control and Sustainable Cultivation of Vegetables. Publisher Copyright: © 2020 Society of Chemical Industry

PY - 2020/7/1

Y1 - 2020/7/1

N2 - BACKGROUND: Tomato spotted wilt orthotospovirus (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 influences the reproduction of its vector to enhance transmission and whether infection with TSWV changes the mating behavior of F. occidentalis are not fully understood. RESULTS: TSWV-exposed thrips had a significantly longer developmental time than non-exposed individuals. More importantly, increased developmental time was predominantly associated with adults, a stage critical for dispersal and virus transmission. In addition, 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 female/male ratio of progeny shifted from 1.3–7.0/1 to 0.6–1.1/1. As for mating behavior, copulation time was significantly longer in TSWV-exposed thrips. Finally, females tended to re-mate less when exposed to the virus. Resistance to re-mating may lead to reduced sperm availability in females, which translates to a larger number of male progeny under a haplodiploid system. CONCLUSION: These combined results suggest that TSWV can influence the developmental time, mating behavior, fecundity, and offspring sex allocation of its vector F. occidentalis to facilitate virus transmission. As such, a monitoring program capable of the earlier detection of the virus in host plants and/or its insect vector, thrips, using double-antibody sandwich enzyme-linked immunosorbent assay (DAS-ELISA), real time quantitative polymerase chain reaction (RT-qPCR) or virus detection strips might be beneficial for long-term, sustainable management.

AB - BACKGROUND: Tomato spotted wilt orthotospovirus (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 influences the reproduction of its vector to enhance transmission and whether infection with TSWV changes the mating behavior of F. occidentalis are not fully understood. RESULTS: TSWV-exposed thrips had a significantly longer developmental time than non-exposed individuals. More importantly, increased developmental time was predominantly associated with adults, a stage critical for dispersal and virus transmission. In addition, 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 female/male ratio of progeny shifted from 1.3–7.0/1 to 0.6–1.1/1. As for mating behavior, copulation time was significantly longer in TSWV-exposed thrips. Finally, females tended to re-mate less when exposed to the virus. Resistance to re-mating may lead to reduced sperm availability in females, which translates to a larger number of male progeny under a haplodiploid system. CONCLUSION: These combined results suggest that TSWV can influence the developmental time, mating behavior, fecundity, and offspring sex allocation of its vector F. occidentalis to facilitate virus transmission. As such, a monitoring program capable of the earlier detection of the virus in host plants and/or its insect vector, thrips, using double-antibody sandwich enzyme-linked immunosorbent assay (DAS-ELISA), real time quantitative polymerase chain reaction (RT-qPCR) or virus detection strips might be beneficial for long-term, sustainable management.

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KW - mating behavior

KW - sex ratio allocation

KW - tomato spotted wilt orthotospovirus

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Tomato spotted wilt orthotospovirus influences the reproduction of its insect vector, western flower thrips, Frankliniella occidentalis, to facilitate transmission

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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