1887

Abstract

Behavioural fever is a widely conserved response to infection. The host increases body temperature ( ) by altering their preferred temperature ( ), generating a fever and delaying or avoiding pathogen-induced mortality. This response is not ubiquitous in insects, however, although few studies have investigated this response to viral infection. Here, we examined the change in of in response to virus infection using a thermal gradient. No difference in was observed. We suggest that the lack of behavioural fever could be due to the increased energy cost of maintaining a higher whilst the immune response is active. To the best of our knowledge, this is the first study to assay for changes in of infected .

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000296
2015-12-01
2020-09-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/12/3667.html?itemId=/content/journal/jgv/10.1099/jgv.0.000296&mimeType=html&fmt=ahah

References

  1. Adamo S. A. 1998; The specificity of behavioral fever in the cricket Acheta domesticus . J Parasitol 84:529–533 [CrossRef][PubMed]
    [Google Scholar]
  2. Anderson R. D., Blanford S., Thomas M. B. 2013; House flies delay fungal infection by fevering: at a cost. Ecol Entomol 38:1–10 [CrossRef]
    [Google Scholar]
  3. Ardia D. R., Gantz J. E., Schneider B. C., Strebel S. 2012; Costs of immunity in insects: an induced immune response increases metabolic rate and decreases antimicrobial activity. Funct Ecol 26:732–739 [CrossRef]
    [Google Scholar]
  4. Arnold P. A., Johnson K. N., White C. R. 2013; Physiological and metabolic consequences of viral infection in Drosophila melanogaster . J Exp Biol 216:3350–3357 [CrossRef][PubMed]
    [Google Scholar]
  5. Blanford S., Thomas M. B. 2001; Adult survival, maturation, and reproduction of the desert locust Schistocerca gregaria infected with the fungus Metarhizium anisopliae var acridum . J Invertebr Pathol 78:1–8 [CrossRef][PubMed]
    [Google Scholar]
  6. Blanford S., Thomas M. B., Langewald J. 1998; Behavioural fever in the Senegalese grasshopper, Oedaleus senegalensis, and its implications for biological control using pathogens. Ecol Entomol 23:9–14 [CrossRef]
    [Google Scholar]
  7. Boorstein S. M., Ewald P. W. 1987; Costs and benefits of behavioral fever in Melanoplus sanguinipes infected by Nosema acridophagus . Physiol Zool 60:586–595
    [Google Scholar]
  8. Bundey S., Raymond S., Dean P., Roberts S. K., Dillon R. J., Charnley A. K. 2003; Eicosanoid involvement in the regulation of behavioral fever in the desert locust, Schistocerca gregaria . Arch Insect Biochem Physiol 52:183–192 [CrossRef][PubMed]
    [Google Scholar]
  9. Cevallos R. C., Sarnow P. 2010; Temperature protects insect cells from infection by cricket paralysis virus. J Virol 84:1652–1655 [CrossRef][PubMed]
    [Google Scholar]
  10. Chtarbanova S., Lamiable O., Lee K. -Z., Galiana D., Troxler L., Meignin C., Hetru C., Hoffmann J. A., Daeffler L., Imler J. -L. 2014; Drosophila C virus systemic infection leads to intestinal obstruction. J Virol 88:14057–14069 [CrossRef][PubMed]
    [Google Scholar]
  11. Covert J. B., Reynolds W. W. 1977; Survival value of fever in fish. Nature 267:43–45 [CrossRef][PubMed]
    [Google Scholar]
  12. Dillon M. E., Wang G., Garrity P. A., Huey R. B. 2009; Thermal preference in Drosophila . J Therm Biol 34:109–119 [CrossRef][PubMed]
    [Google Scholar]
  13. Dostert C., Jouanguy E., Irving P., Troxler L., Galiana-Arnoux D., Hetru C., Hoffmann J. A., Imler J. L. 2005; The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of Drosophila . Nat Immunol 6:946–953 [CrossRef][PubMed]
    [Google Scholar]
  14. Ekesi S., Maniania N. K., Ampong-Nyarko K. 1999; Effect of temperature on germination, radial growth and virulence of Metarhizium anisopliae and Beauveria bassiana on Megalurothrips sjostedti . Biocontrol Sci Technol 9:177–185 [CrossRef]
    [Google Scholar]
  15. Elliot S. L., Blanford S., Thomas M. B. 2002; Host–pathogen interactions in a varying environment: temperature, behavioural fever and fitness. Proc Biol Sci 269:1599–1607 [CrossRef][PubMed]
    [Google Scholar]
  16. Frid L., Myers J. H. 2002; Thermal ecology of western tent caterpillars Malacosoma californicum pluviale and infection by nucleopolyhedrovirus. Ecol Entomol 27:665–673 [CrossRef]
    [Google Scholar]
  17. Gilchrist G. W., Huey R. B., Partridge L. 1997; Thermal sensitivity of Drosophila melanogaster: evolutionary responses of adults and eggs to laboratory natural selection at different temperatures. Physiol Zool 70:403–414 [CrossRef][PubMed]
    [Google Scholar]
  18. Goda T., Leslie J. R., Hamada F. N. 2014; Design and analysis of temperature preference behavior and its circadian rhythm in Drosophila . J Vis Exp 83:e51097[PubMed]
    [Google Scholar]
  19. Granja C. B., Aranguren L. F., Vidal O. M., Aragón L., Salazar M. 2003; Does hyperthermia increase apoptosis in white spot syndrome virus (WSSV)-infected Litopenaeus vannamei?. Dis Aquat Organ 54:73–78 [CrossRef][PubMed]
    [Google Scholar]
  20. Hamada F. N., Rosenzweig M., Kang K., Pulver S. R., Ghezzi A., Jegla T. J., Garrity P. A. 2008; An internal thermal sensor controlling temperature preference in Drosophila . Nature 454:217–220 [CrossRef][PubMed]
    [Google Scholar]
  21. Hedges L. M., Johnson K. N. 2008; Induction of host defence responses by Drosophila C virus. J Gen Virol 89:1497–1501 [CrossRef][PubMed]
    [Google Scholar]
  22. Huey R. B., Crill W. D., Kingsolver J. G., Weber K. E. 1992; A method for rapid measurement of heat or cold resistance of small insects. Funct Ecol 6:489–494 [CrossRef]
    [Google Scholar]
  23. Huszar T., Imler J. L. 2008; Drosophila viruses and the study of antiviral host-defense. Adv Virus Res 72:227–265 [CrossRef][PubMed]
    [Google Scholar]
  24. Inglis G. D., Johnson D. L., Goettel M. S. 1996; Effects of temperature and thermoregulation on mycosis by Beauveria bassiana in grasshoppers. Biol Control 7:131–139 [CrossRef]
    [Google Scholar]
  25. Kaneko H., Head L. M., Ling J., Tang X., Liu Y., Hardin P. E., Emery P., Hamada F. N. 2012; Circadian rhythm of temperature preference and its neural control in Drosophila . Curr Biol 22:1851–1857 [CrossRef][PubMed]
    [Google Scholar]
  26. Kemp C., Imler J. -L. 2009; Antiviral immunity in Drosophila . Curr Opin Immunol 21:3–9 [CrossRef][PubMed]
    [Google Scholar]
  27. Kluger M. J. 1979; Fever in ectotherms: evolutionary implications. Am Zool 19:295–304 [CrossRef]
    [Google Scholar]
  28. Kluger M. J., Ringler D. H., Anver M. R. 1975; Fever and survival. Science 188:166–168 [CrossRef][PubMed]
    [Google Scholar]
  29. Kobayashi M., Inagaki S., Kawase S. 1981; Effect of high temperature on the development of nuclear polyhedrosis virus in the silkworm, Bombyx mori . J Invertebr Pathol 38:386–394 [CrossRef]
    [Google Scholar]
  30. Lemaitre B., Hoffmann J. 2007; The host defense of Drosophila melanogaster . Annu Rev Immunol 25:697–743 [CrossRef]
    [Google Scholar]
  31. Little T. J., Kraaijeveld A. R. 2004; Ecological and evolutionary implications of immunological priming in invertebrates. Trends Ecol Evol 19:58–60 [CrossRef][PubMed]
    [Google Scholar]
  32. Moore N. F., Pullin J. S. K., Reavy B. 1981; Inhibition of the induction of heat shock proteins in Drosophila melanogaster cells infected with insect picornaviruses. FEBS Lett 128:93–96 [CrossRef][PubMed]
    [Google Scholar]
  33. Moore N. F., Pullin J. S. K., Crump W. A. L., Plus N. 1982; The proteins expressed by different isolates of Drosophila C virus. Arch Virol 74:21–30 [CrossRef][PubMed]
    [Google Scholar]
  34. Nespolo R. F., Lardies M. A., Bozinovic F. 2003; Intrapopulational variation in the standard metabolic rate of insects: repeatability, thermal dependence and sensitivity (Q10) of oxygen consumption in a cricket. J Exp Biol 206:4309–4315 [CrossRef][PubMed]
    [Google Scholar]
  35. Ouedraogo R. M., Cusson M., Goettel M. S., Brodeur J. 2003; Inhibition of fungal growth in thermoregulating locusts, Locusta migratoria, infected by the fungus Metarhizium anisopliae var acridum . J Invertebr Pathol 82:103–109 [CrossRef][PubMed]
    [Google Scholar]
  36. Ouedraogo R. M., Goettel M. S., Brodeur J. 2004; Behavioral thermoregulation in the migratory locust: a therapy to overcome fungal infection. Oecologia 138:312–319 [CrossRef][PubMed]
    [Google Scholar]
  37. Parsons P. A. 1979; Resistance of the sibling species Drosophila melanogaster and Drosophila simulans to high temperatures in relation to humidity: evolutionary implications. Evolution 33:131–136 [CrossRef]
    [Google Scholar]
  38. Prince G. J., Parsons P. A. 1977; Adaptive behaviour of Drosophila adults in relation to temperature and humidity. Aust J Zool 25:285–290 [CrossRef]
    [Google Scholar]
  39. R Development Core Team 2013 R: A Language and Environment for Statistical Computing Vienna: R Foundation for Statistical Computing;
    [Google Scholar]
  40. Sayeed O., Benzer S. 1996; Behavioral genetics of thermosensation and hygrosensation in Drosophila . Proc Natl Acad Sci USA 93:6079–6084 [CrossRef][PubMed]
    [Google Scholar]
  41. Shirasu-Hiza M. M., Schneider D. S. 2007; Confronting physiology: how do infected flies die?. Cell Microbiol 9:2775–2783 [CrossRef][PubMed]
    [Google Scholar]
  42. Stahlschmidt Z. R., Adamo S. A. 2013; Context dependency and generality of fever in insects. Naturwissenschaften 100:691–696 [CrossRef][PubMed]
    [Google Scholar]
  43. Thomas M. B., Blanford S. 2003; Thermal biology in insect–parasite interactions. Trends Ecol Evol 18:344–350 [CrossRef]
    [Google Scholar]
  44. Wasik B. R., Turner P. E. 2013; On the biological success of viruses. Annu Rev Microbiol 67:519–541 [CrossRef][PubMed]
    [Google Scholar]
  45. Xu J., Cherry S. 2014; Viruses and antiviral immunity in Drosophila . Dev Comp Immunol 42:67–84 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000296
Loading
/content/journal/jgv/10.1099/jgv.0.000296
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error