1887

Abstract

Rodent gammaherpesviruses have become important models for understanding human herpesvirus diseases. In particular, interactions between murid herpesvirus 4 and (a non-natural host species) have been extensively studied under controlled laboratory conditions. However, several fundamental aspects of murine gammaherpesvirus biology are not well understood, including how these viruses are transmitted from host to host, and their impacts on host fitness under natural conditions. Here, we investigate the epidemiology of a gammaherpesvirus in free-living wood mice () and bank voles () in a 2-year longitudinal study. Wood mouse herpesvirus (WMHV) was the only herpesvirus detected and occurred frequently in wood mice and also less commonly in bank voles. Strikingly, WMHV infection probability was highest in reproductively active, heavy male mice. Infection risk also showed a repeatable seasonal pattern, peaking in spring and declining through the summer. We show that this seasonal decline can be at least partly attributed to reduced recapture of WMHV-infected adults. These results suggest that male reproductive behaviours could provide an important natural route of transmission for these viruses. They also suggest that gammaherpesvirus infection may have significant detrimental effects in wild hosts, questioning the view that these viruses have limited impacts in natural, co-evolved host species.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.044826-0
2012-11-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/11/2447.html?itemId=/content/journal/jgv/10.1099/vir.0.044826-0&mimeType=html&fmt=ahah

References

  1. Ackermann M. 2006; Pathogenesis of gammaherpesvirus infections. Vet Microbiol 113:211–222 [View Article][PubMed]
    [Google Scholar]
  2. Anderson R. M., May R. M. 1982; Coevolution of hosts and parasites. Parasitology 85:411–426 [View Article][PubMed]
    [Google Scholar]
  3. Barton E. S., White D. W., Cathelyn J. S., Brett-McClellan K. A., Engle M., Diamond M. S., Miller V. L., Virgin H. W. IV 2007; Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 447:326–329 [View Article][PubMed]
    [Google Scholar]
  4. Begon M., Hazel S. M., Baxby D., Bown K. J., Cavanagh R., Chantrey J., Jones T., Bennett M. 1999; Transmission dynamics of a zoonotic pathogen within and between wildlife host species. Proc Biol Sci 266:1939–1945 [View Article][PubMed]
    [Google Scholar]
  5. Behnke J. M., Lewis J. W., Zain S. N., Gilbert F. S. 1999; Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. J Helminthol 73:31–44[PubMed]
    [Google Scholar]
  6. Bennett S. G., Webb J. P. Jr, Madon M. B., Childs J. E., Ksiazek T. G., Torrez-Martinez N., Hjelle B. 1999; Hantavirus (Bunyaviridae) infections in rodents from Orange and San Diego counties, California. Am J Trop Med Hyg 60:75–84[PubMed]
    [Google Scholar]
  7. Bertrand S., Criscuolo F., Faivre B., Sorci G. 2006; Immune activation increases susceptibility to oxidative tissue damage in Zebra Finches. Funct Ecol 20:1022–1027 [View Article]
    [Google Scholar]
  8. Birtles R. J., Hazel S. M., Bennett M., Bown K. J., Raoult D., Begon M. 2001; Longitudinal monitoring of the dynamics of infections due to Bartonella species in UK woodland rodents. Epidemiol Infect 126:323–329 [View Article][PubMed]
    [Google Scholar]
  9. Blasdell K., McCracken C., Morris A., Nash A. A., Begon M., Bennett M., Stewart J. P. 2003; The wood mouse is a natural host for Murid herpesvirus 4. J Gen Virol 84:111–113 [View Article][PubMed]
    [Google Scholar]
  10. Blaskovic D., Stanceková M., Svobodová J., Mistríková J. 1980; Isolation of five strains of herpesviruses from two species of free living small rodents. Acta Virol 24:468[PubMed]
    [Google Scholar]
  11. Booth W., Montgomery W. I., Prodöhl P. A. 2007; Polyandry by wood mice in natural populations. J Zool (Lond) 273:176–182 [View Article]
    [Google Scholar]
  12. Botten J., Mirowsky K., Ye C., Gottlieb K., Saavedra M., Ponce L., Hjelle B. 2002; Shedding and intracage transmission of Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus) model. J Virol 76:7587–7594 [View Article][PubMed]
    [Google Scholar]
  13. Calisher C. H., Wagoner K. D., Amman B. R., Root J. J., Douglass R. J., Kuenzi A. J., Abbott K. D., Parmenter C., Yates T. L. other authors 2007; Demographic factors associated with prevalence of antibody to Sin Nombre virus in deer mice in the western United States. J Wildl Dis 43:1–11[PubMed] [CrossRef]
    [Google Scholar]
  14. Davison A. J. 2002; Evolution of the herpesviruses. Vet Microbiol 86:69–88 [View Article][PubMed]
    [Google Scholar]
  15. Douglass R. J., Wilson T., Semmens W. J., Zanto S. N., Bond C. W., Van Horn R. C., Mills J. N. 2001; Longitudinal studies of Sin Nombre virus in deer mouse-dominated ecosystems of Montana. Am J Trop Med Hyg 65:33–41[PubMed]
    [Google Scholar]
  16. Ehlers B., Küchler J., Yasmum N., Dural G., Voigt S., Schmidt-Chanasit J., Jäkel T., Matuschka F.-R., Richter D. other authors 2007; Identification of novel rodent herpesviruses, including the first gammaherpesvirus of Mus musculus . J Virol 81:8091–8100 [View Article][PubMed]
    [Google Scholar]
  17. Ehlers B., Dural G., Yasmum N., Lembo T., de Thoisy B., Ryser-Degiorgis M.-P., Ulrich R. G., McGeoch D. J. 2008; Novel mammalian herpesviruses and lineages within the Gammaherpesvirinae: cospeciation and interspecies transfer. J Virol 82:3509–3516 [View Article][PubMed]
    [Google Scholar]
  18. Eraud C., Duriez O., Chastel O., Faivre B. 2005; The energetic cost of humoral immunity in the collared dove, Streptopelia decaocto: is the magnitude sufficient to force energy-based trade-offs?. Funct Ecol 19:110–118 [View Article]
    [Google Scholar]
  19. Ezenwa V. O., Ekernas L. S., Creel S. 2012; Unravelling complex associations between testosterone and parasite infection in the wild. Funct Ecol 26:123–133 [View Article]
    [Google Scholar]
  20. Ficová M., Betáková T., Pančík P., Václav R., Prokop P., Halásová Z., Kúdelová M. 2011; Molecular detection of murine herpesvirus 68 in ticks feeding on free-living reptiles. Microb Ecol 62:862–867 [View Article][PubMed]
    [Google Scholar]
  21. Folstad I., Karter A. 1992; Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622 [View Article]
    [Google Scholar]
  22. Fortier G., van Erck E., Pronost S., Lekeux P., Thiry E. 2010; Equine gammaherpesviruses: pathogenesis, epidemiology and diagnosis. Vet J 186:148–156 [View Article][PubMed]
    [Google Scholar]
  23. François S., Vidick S., Sarlet M., Michaux J., Koteja P., Desmecht D., Stevenson P. G., Vanderplasschen A., Gillet L. 2010; Comparative study of murid gammaherpesvirus 4 infection in mice and in a natural host, bank voles. J Gen Virol 91:2553–2563 [View Article][PubMed]
    [Google Scholar]
  24. Frank S. A. 1996; Models of parasite virulence. Q Rev Biol 71:37–78 [View Article][PubMed]
    [Google Scholar]
  25. Gouveia-Oliveira R., Pedersen A. G. 2009; Higher variability in the number of sexual partners in males can contribute to a higher prevalence of sexually transmitted diseases in females. J Theor Biol 261:100–106 [View Article][PubMed]
    [Google Scholar]
  26. Hanssen S. A. 2006; Costs of an immune challenge and terminal investment in a long-lived bird. Ecology 87:2440–2446 [View Article][PubMed]
    [Google Scholar]
  27. Hinson E. R., Shone S. M., Zink M. C., Glass G. E., Klein S. L. 2004; Wounding: the primary mode of Seoul virus transmission among male Norway rats. Am J Trop Med Hyg 70:310–317[PubMed]
    [Google Scholar]
  28. Hricová M., Mistríková J. 2008; Ecological characterization of murine gammaherpesvirus 68 and it’s epidemiological implications. Biologia 63:753–755 [View Article]
    [Google Scholar]
  29. Hughes D. J., Kipar A., Sample J. T., Stewart J. P. 2010a; Pathogenesis of a model gammaherpesvirus in a natural host. J Virol 84:3949–3961 [View Article][PubMed]
    [Google Scholar]
  30. Hughes D. J., Kipar A., Milligan S. G., Cunningham C., Sanders M., Quail M. A., Rajandream M.-A., Efstathiou S., Bowden R. J. other authors 2010b; Characterization of a novel wood mouse virus related to murid herpesvirus 4. J Gen Virol 91:867–879 [View Article][PubMed]
    [Google Scholar]
  31. Hughes D. J., Kipar A., Leeming G. H., Bennett E., Howarth D., Cummerson J. A., Papoula-Pereira R., Flanagan B. F., Sample J. T., Stewart J. P. 2011; Chemokine binding protein M3 of murine gammaherpesvirus 68 modulates the host response to infection in a natural host. PLoS Pathog 7:e1001321 [View Article][PubMed]
    [Google Scholar]
  32. Kallio E. R., Poikonen A., Vaheri A., Vapalahti O., Henttonen H., Koskela E., Mappes T. 2006; Maternal antibodies postpone hantavirus infection and enhance individual breeding success. Proc Biol Sci 273:2771–2776 [View Article][PubMed]
    [Google Scholar]
  33. Klein S. L. 2004; Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26:247–264 [View Article][PubMed]
    [Google Scholar]
  34. Lehmer E. M., Jones J. D., Bego M. G., Varner J. M., Jeor S. S., Clay C. A., Dearing M. D. 2010; Long-term patterns of immune investment by wild deer mice infected with Sin Nombre virus. Physiol Biochem Zool 83:847–857 [View Article][PubMed]
    [Google Scholar]
  35. Mackey K., Steinkamp A., Chomczynski P. 1998; DNA extraction from small blood volumes and the processing of cellulose blood cards for use in polymerase chain reaction. Mol Biotechnol 9:1–5 [View Article][PubMed]
    [Google Scholar]
  36. McCormick C., Ganem D. 2005; The kaposin B protein of KSHV activates the p38/MK2 pathway and stabilizes cytokine mRNAs. Science 307:739–741 [View Article][PubMed]
    [Google Scholar]
  37. Milho R., Smith C. M., Marques S., Alenquer M., May J. S., Gillet L., Gaspar M., Efstathiou S., Simas J. P., Stevenson P. G. 2009; In vivo imaging of murid herpesvirus-4 infection. J Gen Virol 90:21–32 [View Article][PubMed]
    [Google Scholar]
  38. Mills J. N., Ksiazek T. G., Ellis B. A., Rollin P. E., Nichol S. T., Yates T. L., Gannon W. L., Levy C. E., Engelthaler D. M. other authors 1997; Patterns of association with host and habitat: antibody reactive with Sin Nombre virus in small mammals in the major biotic communities of the southwestern United States. Am J Trop Med Hyg 56:273–284[PubMed]
    [Google Scholar]
  39. R Development Core Team. 2011; R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
    [Google Scholar]
  40. Randolph S. 1977; Changing spatial relationships in a population of Apodemus sylvaticus with onset of breeding. J Anim Ecol 46:653–676 [View Article]
    [Google Scholar]
  41. Roberts M., Buchanan K., Evans M. 2004; Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239 [View Article]
    [Google Scholar]
  42. Simas J. P., Efstathiou S. 1998; Murine gammaherpesvirus 68: a model for the study of gammaherpesvirus pathogenesis. Trends Microbiol 6:276–282 [View Article][PubMed]
    [Google Scholar]
  43. Sunil-Chandra N. P., Efstathiou S., Nash A. A. 1992; Murine gammaherpesvirus 68 establishes a latent infection in mouse B lymphocytes in vivo . J Gen Virol 73:3275–3279 [View Article][PubMed]
    [Google Scholar]
  44. Telfer S., Bennett M., Bown K. J., Carslake D., Cavanagh R., Hazel S. M., Jones T., Begon M. 2005; Infection with cowpox virus decreases female maturation rates in wild populations of woodland rodents. Oikos 109:317–322 [View Article]
    [Google Scholar]
  45. Telfer S., Bennett M., Carslake D., Helyar S., Begon M. 2007; The dynamics of murid gammaherpesvirus 4 within wild, sympatric populations of bank voles and wood mice. J Wildl Dis 43:32–39[PubMed] [CrossRef]
    [Google Scholar]
  46. Thrall P. H., Antonovics J., Dobson A. P. 2000; Sexually transmitted diseases in polygynous mating systems: prevalence and impact on reproductive success. Proc Biol Sci 267:1555–1563 [View Article][PubMed]
    [Google Scholar]
  47. Weck K. E., Barkon M. L., Yoo L. I., Speck S. H., Virgin HW I. V. 1996; Mature B cells are required for acute splenic infection, but not for establishment of latency, by murine gammaherpesvirus 68. J Virol 70:6775–6780[PubMed]
    [Google Scholar]
  48. White D. W., Keppel C. R., Schneider S. E., Reese T. A., Coder J., Payton J. E., Ley T. J., Virgin H. W., Fehniger T. A. 2010; Latent herpesvirus infection arms NK cells. Blood 115:4377–4383 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.044826-0
Loading
/content/journal/jgv/10.1099/vir.0.044826-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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