Arthropod-Plant Interactions

, Volume 9, Issue 2, pp 107–120 | Cite as

Modelling transmission characteristics and epidemic development of the tospovirus–thrip interaction

Original Paper


Tospoviruses are plant viruses in the genus Bunyaviridae transmitted in a persistent–propagative manner by a range of thrips species and cause disease in wide range of cultivated crops and wild hosts. The viruses in this genus are the only plant-infecting members of the Bunyaviridae. A distinguishing feature, of tospoviruses, from other persistent–propagative plant viruses is that acquisition from infected host plants only occurs by larvae of thrips species. This transmission characteristic is modelled generically as acquisition by juveniles, an invasion threshold is derived, and the dynamics of the system are compared with systems where adults only are involved in acquisition and inoculation. The comparison suggests that in the model disease develops faster and to a greater extent where adults are involved in both acquisition and inoculation. In that case, mobile non-viruliferous adults visit infected plants to acquire virus and in turn visit healthy plants to inoculate virus, whereas acquisition by non-mobile juveniles depends firstly on eggs being laid on an infected plant and then on the virus passaging trans-stadially from the juvenile to the mobile adult form: other factors being equal, the greater the mobility of vectors the greater the probability of both acquisition and inoculation. Where acquisition is by both juvenile and adult forms of the vector, the derived invasion threshold is simply the sum of the component thresholds for each life stage; however, there may be a fitness cost on combining these characteristics expressed as a trade-off between optimising the life history parameters involved in each acquisition route.


Virus–vector association Virus acquisition Virus inoculation Trans-stadial transmission Invasion threshold Fitness cost Life history trade-offs 


  1. Amaku M, Burattini MN, Coutinho FAB, Massad E (2010) Modelling the competition between viruses in a complex plant-pathogen system. Phytopathology 100:1042–1047Google Scholar
  2. Bautista RC, Mau RFL, Cho JJ, Custer DM (1995) Potential of tomato spotted wilt plant nests in Hawaii as virus reservoirs for transmission by Frankliniella occidentalis (Thysanoptera: Thripidae). Phytopathology 85:953–958CrossRefGoogle Scholar
  3. Belliure B, Janssen A, Maris PC, Peters D, Sabelis MW (2005) Herbivore arthropods benefit from vectoring plant viruses. Ecol Lett 8:70–79CrossRefGoogle Scholar
  4. Bourhy H, Cowley JA, Larrous F, Holmes EC, Walker PJ (2005) Phylogenetic relationships among rhabdoviruses inferred using the L polymerase gene. J Gen Virol 86:2849–2858Google Scholar
  5. Bragard C, Caciagli P, Lemaire O, Lopez-Moya LL, MacFarlane S, Peters D, Susi P, Torrence L (2013) Status and prospects of plant virus control through interference with vector transmission. Annu Rev Phytopathol 51:177–201CrossRefPubMedGoogle Scholar
  6. Caswell H (2001) Matrix population models: construction, analysis and interpretation, 2nd edn. Sinauer Associates, SunderlandGoogle Scholar
  7. Chatzivassiliou EK, Peters D, Katis NI (2002) The efficiency by which Thrips palmi transmit Tomato spotted wilt virus depends on their host preference and reproductive strategy. Phytopathology 92:603–609CrossRefPubMedGoogle Scholar
  8. Chatzivassiliou EK, Peters D, Katis NI (2007) The role of weeds in the spread of Tomato spotted wilt virus by Thrips tabaci (Thysanoptera: Thripidae) in tobacco. J Phytopathol 155:699–705CrossRefGoogle Scholar
  9. Childers CC, Kitajima EW, Welbourn WC, Rivers C, Ochoa R (2001) Brevipalpus mites on citrus and their status as vectors of citrus leprosis. Manejo Integrado de Plagas (Costa Rica) 60:66–70Google Scholar
  10. De Assis FM, Deom CA, Sherwood JL (2004) Acquisition of Tomato spotted wilt virus by adults of two thrips species. Phytopathology 94:333–336CrossRefGoogle Scholar
  11. DeAngelis JD, Sether DM, Rossignol PA (1993) Survival, development, and reproduction in western flower thrips (Thysanoptera: Thripidae) exposed to Impatiens necrotic spot virus. Environ Entomol 22(6):1308–1312CrossRefGoogle Scholar
  12. Edelstein-Keshet L (1988) Mathematical models in biology. Random House, New YorkGoogle Scholar
  13. Fabre F, Chadoeuf J, Costa C, Lecoq H, Desbiez C (2010) Asymmetrical over-infection as a process of plant virus emergence. J Theor Biol 265:377–388Google Scholar
  14. German TL, Ullman DE, Moyer JW (1992) Tospoviruses: diagnosis, molecular biology, phylogeny, and vector relationships. Annu Rev Phytopathol 30:315–348CrossRefPubMedGoogle Scholar
  15. Gibb KS, Randles JW (1991) Transmission of velvet tobacco mottle virus and related viruses by the Mirid Cyrtopeltis nicotianae. Adv Dis Vect Res 7:1–18Google Scholar
  16. Gray SM, Banerjee N (1999) Mechanisms of arthropod transmission of plant and animal viruses. Microbiol Mol Biol Rev 63:128–148PubMedCentralPubMedGoogle Scholar
  17. Hogenhout SA, Ammar ED, Whitfield AE, Redinbaugh MG (2008) Insect vector associations with persistently transmitted viruses. Annu Rev Phytopathol 46:327–359CrossRefPubMedGoogle Scholar
  18. Ingwell LL, Eigenbrode SD, Bosque-Perez NA (2012) Plant viruses alter insect behaviour to enhance their spread. Sci Rep 2:1–6CrossRefGoogle Scholar
  19. Inoue T, Sakurai T (2007) The phylogeny of Thrips (Thysanoptera: Thripidae) based on partial sequences of cytochrome oxidase I, 28S ribosomal DNA and elongation factor-1α and the association with vector competences of tospoviruses. Appl Entomol Zool 42:71–81Google Scholar
  20. Inoue T, Sakurai T, Murai T, Maeda T (2004) Specificity of accumulation and transmission of tomato spotted wilt virus (TSWV) in two genera, Frankliniella and Thrips (Thysanopter: P Thripidae). Bull Entomol Res 94:501–507CrossRefPubMedGoogle Scholar
  21. Jeger MJ, van den Bosch F, Madden LV, Holt J (1998) A model for analysing plant–virus transmission characteristics and epidemic development. IMA J Math Appl Med Biol 15:1–18CrossRefGoogle Scholar
  22. Jeger MJ, Holt J, van den Bosch F, Madden LV (2004) Epidemiology of insect-transmitted viruses: modelling disease dynamics and control interventions. Physiol Entomol 29:291–304CrossRefGoogle Scholar
  23. Jeger MJ, Seal SE, van den Bosch F (2006) Evolutionary epidemiology of plant virus disease. Adv Plant Virus Res 67:164–203Google Scholar
  24. Jeger MJ, Madden LV, van den Bosch F (2009) The effect of virus transmission route on plant virus epidemic development and disease control. J Theor Biol 258:198–207CrossRefPubMedGoogle Scholar
  25. Jeger MJ, Chen Z, Powell G, Hodge S, van den Bosch F (2011) Interactions in a host plant–virus–vector–parasitoid system: modelling the consequences for virus transmission and disease dynamics. Virus Res 159:183–193CrossRefPubMedGoogle Scholar
  26. Kritzman A, Gera A, Raccah B, van Lent JWM, Peters D (2002) The route of Tomato spotted wilt virus inside the thrips body in relation to transmission efficiency. Arch Virol 147:2143–2156CrossRefPubMedGoogle Scholar
  27. Lafforgue G, Sardanyes J, Elena SF (2011) Differences in accumulation and virulence determine the outcome of competition during Tobacco etch virus coinfection. PLOS ONE 6:e17917Google Scholar
  28. Madden LV, Jeger MJ, van den Bosch F (2000) A theoretical assessment of the effects of vector–virus transmission mechanism on plant virus disease epidemics. Phytopathology 90:576–594CrossRefPubMedGoogle Scholar
  29. Maris PC, Joosten NN, Goldbach RW, Peters D (2004) Tomato spotted wilt virus infection improves host suitability for its vector Frankliniella occidentalis. Phytopathology 94:706–711CrossRefPubMedGoogle Scholar
  30. Moritz G, Kumm S, Mound L (2004) Tospovirus transmission depends on thrips ontogeny. Virus Res 100:143–149CrossRefPubMedGoogle Scholar
  31. Moury B, Fabre F, Montarry J, Janzac B, Ayme V, Palloix A (2010) The adapation of plant viruses to varietal resistances. Virologie 14:227–239Google Scholar
  32. Nagata T, Inoue-Nagata AK, Smid HM, Goldbach R, Peters D (1999) Tissue tropism related to vector competence of Frankliniella occidentalis for tomato spotted wilt tospovirus. J Gen Virol 80:507–515Google Scholar
  33. Nagata T, Inoue-Nagata AK, van Lent J, Goldbach R, Peters D (2002) Factors determining vector competence and specificity for transmission of Tomato spotted wilt virus. J Gen Virol 83:663–671PubMedGoogle Scholar
  34. Okasaki S, Okuda M, Sakurai T (2009) Evaluation of weed species as Tomato spotted wilt virus (Bunyaviridae: Tospovirus) acquisition sources for Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Jpn J Entomol Zool 53:181–184CrossRefGoogle Scholar
  35. Okasaki S, Okuda M, Komi K, Yamasaki S, Okuda S, Sakurai T, Iwanami T (2011) The effect of virus titre on acquisition efficiency of Tomato spotted wilt virus by Frankliniella occidentalis and the effect of temperature on detectable period of the virus in dead bodies. Australas Plant Pathol 40:120–125CrossRefGoogle Scholar
  36. Okuda M, Fuji S, Okuda S, Sako K, Iwanami T (2010) Evaluation of the potential of thirty two weed species as infection sources of Impatiens necrotic spot virus. J Plant Pathol 92:357–361Google Scholar
  37. Pappu HR, Jones RAC, Jain RK (2009) Global status of tospovirus epidemics in diverse cropping systems: successes achieved and challenges ahead. Virus Res 141(2):219–236CrossRefPubMedGoogle Scholar
  38. Pu Y, Kikuchi A, Morliyasu Y, Tomaru M, Jin Y et al (2011) Rice dwarf viruses with dysfunctional genomes generated in plants are filtered out in vector insects: implications for the origin of the virus. J Virol 85:2975–2979CrossRefPubMedCentralPubMedGoogle Scholar
  39. Reitz SR, Yearby EL, Funderburk JE, Stavisky J, Momol MT, Olson SM (2003) Integrated management tactics for Frankliniella thrips (Thysanoptera: Thripidae) in field-grown pepper. J Econ Entomol 96(4):1201–1214CrossRefPubMedGoogle Scholar
  40. Roca E, Aramburu J, Moriones E (1997) Comparative host reactions and Frankliniella occidentalis transmission of different isolates of tomato spotted wilt tospovirus from Spain. Plant Pathol 46:407–415CrossRefGoogle Scholar
  41. Rodrigues JCV, Nogueira NL, Freitas DS, Prates HS (1997) Virus-line particles associated with Brevipalpus phoenicis Geijskes (Acari: Tenuipalpidae), vector of Citrus leprosis virus. An Soc Entomol Brasil 26:391–395Google Scholar
  42. Rotenberg D, Krishna Kumar NK, Ullman DE, Montero-Astua M, Willis DK, German TL, Whitfield AE (2009) Variation in Tomato spotted wilt virus titre in Frankliniella occidentalis and its association with frequency of transmission. Phytopathology 99:404–410CrossRefPubMedGoogle Scholar
  43. Sacristan S, Diaz M, Fraile A, Garcia-Arenal F (2011) Contact transmission of Tobacco mosaic virus: a quantitative analysis of parameters relevant for virus evolution. J Virol 85:4974–4981Google Scholar
  44. Sakimura K (1963) Frankliniella fusca, an additional vector for the Tomato spotted wilt virus, with notes on Thrips tabaci, another vector. Phytopathology 53(4):412–415Google Scholar
  45. Scholthof K-BG, Adkins S, Czosnek H, Palukaitis P, Jacquot E, Hohn T, Hohn B, Saunders K, Candresse T, Ahlquist P, Hemenway C, Foster GD (2011) Top 10 plant viruses in molecular plant pathology. Mol Plant Pathol 12:938–954CrossRefPubMedGoogle Scholar
  46. Smith EA, Ditommaso A, Fuchs M, Shelton AM, Nault BA (2011) Weed hosts for onion thrips (Thysanoptera: Thripidae) and their potential role in the epidemiology of Iris yellow spot virus in an onion ecosystem. Environ Entomol 40:194–203CrossRefGoogle Scholar
  47. Stafford CA, Walker GP, Ullman DE (2011) Infection with a plant virus modifies vector feeding behaviour. Proc Natl Acad Sci USA 108:9350–9355CrossRefPubMedCentralPubMedGoogle Scholar
  48. Stumpf F, Kennedy G (2005) Effects of Tomato spotted wilt virus (TSWV) isolates, host plants, and temperature on survival, size, and development time of Frankliniella fusca. Entomol Exp Appl 114(3):215–225CrossRefGoogle Scholar
  49. Stumpf F, Kennedy G (2007) Effects of tomato spotted wilt virus isolates, host plants, and temperature on survival, size, and development time of Frankliniella occidentalis. Entomol Exp Appl 123(2):139–147CrossRefGoogle Scholar
  50. Sundaraj S, Srinivasan AK, Culbreath DG, Riley DG, Pappu HR (2014) Host plant resistance against Tomato spotted wilt virus in peanut (Arachis hypogaea) and its impact on susceptibility to the virus, virus population genetics, and vector feeding behaviour and survival. Phytopathology 104:202–210CrossRefPubMedGoogle Scholar
  51. Tedeschi R, Ciuffo M, Mason G, Roggero P, Tavella L (2001) Transmissibility of four tospoviruses by a thelytokous population of Thrips tabaci from Liguria, northwestern Italy. Phytoparasitica 29:37–45CrossRefGoogle Scholar
  52. Triplehorn CA, Johnson NF (2005) Borror and DeLong’s introduction to the study of insects. Thomson Brooks/Cole, Belmont, pp 401–402Google Scholar
  53. Tsuda S, Fujisawa I, Ohnishi J, Hosokawa D, Tomaru K (1996) Localization of tomato spotted wilt tospovirus in larvae and pupae of the insect vector Thrips setosus. Phytopathology 86:1199–1203CrossRefGoogle Scholar
  54. Tu Z, Ling B, Xu DL, Zhang MX, Zhou GH (2013) Effects of southern rice black-streaked dwarf virus on the development and fecundity of its vector Sogatella furcifera. Virol J 10:Article Number 145Google Scholar
  55. Ullman DE, Cho JJ, Mau RFL, Westcot DM, Custer DM (1992) Midgut epithelial cells act as a barrier to tomato spotted wilt virus acquisition by adult western flower thrips. Phytopathology 82:1333–1342CrossRefGoogle Scholar
  56. Ullman D, Moyer J, Goldbach R, Moritz G, 2007. VIII International Symposium on Thysanoptera and Tospoviruses, September 11–15, 2005, Asilomar, Pacific Grove, California. 49 pp. J Ins Sci 7:28. Scholar
  57. Van den Bosch F, Akudibilah G, Seal SE, Jeger MJ (2006) Host resistance and the evolutionary response of plant viruses. J Appl Ecol 43:506–516CrossRefGoogle Scholar
  58. Van den Bosch F, Jeger MJ, Gilligan CA (2007) Disease control and its selection for damaging plant virus strains in vegetatively propagated staple food crops: a theoretical assessment. Proc Biol Sci 274:11–18CrossRefPubMedCentralPubMedGoogle Scholar
  59. Van den Bosch F, McRoberts N, van den Berg F, Madden LV (2008) The basic reproductive number of plant pathogens: matrix approaches to complex dynamics. Phytopathology 98:239–249CrossRefPubMedGoogle Scholar
  60. Van der Wetering F, Goldbach R, Peters D (1996) Tomato spotted wilt tospovirus ingestion by first instar larvae of Frankliniella occidentalis is a prerequisite for transmission. Phytopathology 86:900–905CrossRefGoogle Scholar
  61. Wang H, Xu D, Pu L, Zhou G (2014) Southern rice black-streaked dwarf virus alters insect vector’s host orientation preferences to enhance spread and increase Rice ragged stunt virus co-infection. Phytopathology 104:196–201CrossRefPubMedGoogle Scholar
  62. Whitfield AE, Ullman DE, German TL (2005) Tospovirus-thrips interactions. Annu Rev Phytopathol 43:459–489CrossRefPubMedGoogle Scholar
  63. Wijkamp I, Goldbach R, Peters P (1996) Propagation of tomato spotted wilt virus in Frankliniella occidentalis does neither result in pathological effects nor in transovarial passage of the virus. Entomol Exp Appl 81:285–292CrossRefGoogle Scholar
  64. Zhang XS, Holt J (2001) Mathematical models of cross protection in the epidemiology of plant-virus diseases. Phytopathology 91:924–934Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Centre for Environmental PolicyImperial College LondonAscotUK
  2. 2.Biomathematics and BioinformaticsRothamsted ResearchHarpendenUK
  3. 3.Plant Pathology DepartmentUniversity of California, DavisDavisUSA

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