Age-related effects of chronic hantavirus infection on female host fecundity

Journal of Animal Ecology

Volumn 84, Issue 5, 2015, Pages 1264-1272

  Kallio, Eva R ^a,b   Helle, Heikki ^a   Koskela, Esa ^a   Mappes, Tapio ^a   Vapalahti, Olli ^c,d,e  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF HELSINKI   (Finland)

^e HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

Disease transmission; Endemic pathogen; Female fecundity; Host pathogen interaction; Resource allocation

Indexed keywords

AGE STRUCTURE; BREEDING SEASON; DISEASE TRANSMISSION; ENDEMIC SPECIES; FECUNDITY; FEMALE BEHAVIOR; FITNESS; HOST-PATHOGEN INTERACTION; INFECTIOUS DISEASE; RESOURCE ALLOCATION; RODENT; VIRAL DISEASE;

FINLAND; KESKI-SUOMI;

ANIMALIA; CLETHRIONOMYS GLAREOLUS; HANTAVIRUS; PUUMALA VIRUS;

AGE; ANIMAL; ARVICOLINAE; FEMALE; FERTILITY; FINLAND; HANTAVIRUS INFECTION; PATHOPHYSIOLOGY; PHYSIOLOGY; PUUMALA VIRUS; REPRODUCTION; RODENT DISEASE; SEASON; VETERINARY;

AGE FACTORS; ANIMALS; ARVICOLINAE; FEMALE; FERTILITY; FINLAND; HANTAVIRUS INFECTIONS; PUUMALA VIRUS; REPRODUCTION; RODENT DISEASES; SEASONS;

EID: 84939256852     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/1365-2656.12387     Document Type: Article

References (74)

1. Amori, G., Hutterer, R., Kryštufek, B., Yigit, N., Mitsain, G., Munoz, L.J.P. et al. (2008) Myodes glareolus. In: IUCN (2013) IUCN red list of threatened species. Version 2013.2. www.iucnredlist.org.
2. Anderson, R.M. & May, R.M. (1978) Regulation and stability of host-parasite population interactions: 1. Regulatory processes. Journal of Animal Ecology, 47, 219-247.
3. Begon, M., Telfer, S., Smith, M.J., Burthe, S., Paterson, S. & Lambin, X. (2008) Seaonal host dynamics drive the timing of recurrent epidemics in a wildlife population. Proceedings of Royal Society B: Biological Sciences, 276, 1603-1610.
4. Beldomenico, P.M. & Begon, M. (2010) Disease spread, susceptibility and infection intensity: vicious circles? Trends in Ecology and Evolution, 25, 21-27.
5. Bernshtein, A.D., Apekina, N.S., Mikhailova, T.V., Myasnikov, Y.A., Khlyap, L.A., Korotkov, Y.S. et al. (1999) Dynamics of Puumala hantavirus infection in naturally infected bank voles (Clethrinomys glareolus). Archives of Virology, 144, 2415-2428.
6. Boulinier, T. & Staszewski, V. (2008) Maternal transfer of antibodies: raising immuno-ecology issues. Trends in Ecology and Evolution, 23, 282-288.
7. Burnham, K.P. & Anderson, D.R. (2000) Model Selection and Inference: A Practical Information-Theoretic Approach. Springer, New York.
8. Burthe, S., Telfer, S., Lambin, X., Bennett, M., Carslake, D., Smith, A. et al. (2006) Cowpox virus infection in natural field vole Microtus agrestis populations: delayed density dependence and individual risk. Journal of Animal Ecology, 75, 1416-1425.
9. Burthe, S., Telfer, S., Begon, M., Bennett, M., Smith, A. & Lambin, X. (2008) Cowpox virus infection in natural field vole Microtus agrestis populations: significant negative impacts on survival. Journal of Animal Ecology, 77, 110-119.
10. Clutton-Brock, T.H. (1984) Reproductive effort and terminal investment in iteroparous animals. The American Naturalist, 123, 212-229.
11. Davis, S., Calvet, E. & Leirs, H. (2005) Fluctuating rodent populations and risk to humans from rodent-borne zoonoses. Vector-Borne and Zoonotic Diseases, 5, 305-314.
12. Dearing, M.D., Previtali, M.A., Jones, J.D., Ely, P.W. & Wood, B.A. (2009) Seasonal variation in Sin Nombre virus infections in deer mice: preliminary results. Journal of Wildlife Diseases, 45, 430-436.
13. Ebenhard, T. (1990) A colonization strategy in the field vole (Microtus agrestis): reproductive traits and body size. Ecology, 71, 1833-1848.
14. Escutenaire, S., Chalon, P., De Jaegere, F., Karelle-Bui, L., Mees, G., Brochier, B. et al. (2002) Behavioral, physiologic, and habitat influences on the dynamics of Puumala virus infection in bank voles (Clethrionomys glareolus). Emerging Infectious Diseases, 8, 930-936.
15. Feore, S.M., Bennett, M., Chantrey, J., Jones, T., Baxby, D. & Begon, M. (1997) The effect of cowpox virus infection on fecundity in bank voles and wood mice. Proceedings of Royal Society B: Biological Sciences, 264, 1457-1461.
16. Forbes, M.R.L. (1993) Parasitism and host reproductive effort. Oikos, 67, 444-450.
17. Forbes, K.M., Stuart, P., Mappes, T., Henttonen, H. & Huitu, O. (2014) Food resources and intestinal parasites as limiting factors for boreal vole populations during winter. Ecology, 95, 3139-3148.
18. Gasparini, J., McCoy, K.D., Haussy, C., Tveraa, T. & Boulinier, T. (2001) Induced maternal response to the Lyme disease spirochaete Borrelia burgdorferi sensu lato in a colonial seabird, the kittiwake Rissa tridactyla. Proceedings of Royal Society B: Biological Sciences, 268, 647-650.
19. Gavrilovskaya, I.N., Apekina, N.S., Bernshtein, A.D., Demina, V.T., Okulova, N.M., Myasnikov, Y.A. et al. (1990) Pathogenesis of hemorrhagic fever with renal syndrome virus infection and mode of horizontal transmission of hantavirus in bank voles. Archives of Virology, Suppl. 1, 57-62.
20. Hakkarainen, H., Huhta, E., Koskela, E., Mappes, T., Soveri, T. & Suorsa, P. (2007) Eimeria-parasites are associated with a lowered mother's and offspring's body condition in island and mainland populations of the bank vole. Parasitology, 134, 23-31.
21. Hansson, L. & Henttonen, H. (1988) Rodent dynamics as community processes. Trends in Ecology and Evolution, 3, 195-200.
22. Huitu, O., Jokinen, I., Korpimäki, E., Koskela, E. & Mappes, T. (2007) Phase dependence in winter physiological condition of cyclic voles. Oikos, 116, 565-577.
23. Jonsson, C.B., Figueiredo, L.T. & Vapalahti, O. (2010) A global perspective on hantavirus ecology, epidemiology, and disease. Clinical Microbiology Reviews, 23, 412-441.
24. Kaitala, V., Mappes, T. & Ylönen, H. (1997) Delayed and suppressed reproduction in equilibrium and chaotic populations. Evolutionary Ecology, 11, 105-126.
25. Kallio, E.R., Klingstrom, J., Gustafsson, E., Manni, T., Vaheri, A., Henttonen, H. et al. (2006a) Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment. Journal of General Virology, 87, 2127-2134.
26. Kallio, E.R., Poikonen, A., Vaheri, A., Vapalahti, O., Henttonen, H., Koskela, E. et al. (2006b) Maternal antibodies postpone hantavirus infection and enhance individual breeding success. Proceedings of Royal Society B: Biological Sciences, 273, 2771-2776.
27. Kallio, E.R., Voutilainen, L., Vapalahti, O., Vaheri, A., Henttonen, H., Koskela, E. et al. (2007) Endemic hantavirus infection impairs the winter survival of its rodent host. Ecology, 88, 1911-1916.
28. Kallio, E.R., Begon, M., Henttonen, H., Koskela, E., Mappes, T., Vaheri, A. et al. (2009) Cyclic hantavirus epidemics in humans - predicted by rodent host dynamics. Epidemics, 1, 101-107.
29. Kallio, E.R., Begon, M., Henttonen, H., Koskela, E., Mappes, T., Vaheri, A. et al. (2010) Hantavirus infections in fluctuating host populations: the role of maternal antibodies. Proceedings of Royal Society B: Biological Sciences, 277, 3783-3791.
30. Kallio, E.R., Henttonen, H., Koskela, E., Lundkvist, A., Mappes, T. & Vapalahti, O. (2013) Sex-based difference in hantavirus transmission dynamics. Biology Letters, 9, 20130887.
31. Kallio, E.R., Begon, M., Birtles, R., Bown, K., Koskela, E., Mappes, T. et al. (2014) First report of Anaplasma phagocytophilum and Babesia microti in rodents in Finland. Vector-Borne and Zoonotic Diseases, 14, 389-393.
32. Kallio, E.R., Helle, H., Koskela, E., Mappes, T. & Vapalahti, O. (2015) Data from: Age-related effects of chronic hantavirus infection on female host. Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.g4q84.
33. Koivula, M., Koskela, E., Mappes, T. & Oksanen, T.A. (2003) Cost of reproduction in the wild: manipulation of reproductive effort in the bank vole. 84. Ecology, 84, 398-405.
34. Korpela, K., Delgado, M.D.M., Henttonen, H., Korpimäki, E., Koskela, E., Ovaskainen, O. et al. (2013) Nonlinear effects of climate on boreal rodent dynamics: mild winters do not negate high-amplitude cycles. Global Change Biology, 19, 697-710.
35. Korpela, K., Helle, P., Henttonen, H., Korpimäki, E., Koskela, E., Ovaskainen, O. et al. (2014) Predator-vole interactions in northern Europe: the role of small mustelids revised. Proceedings of Royal Society B: Biological Sciences, 281, 20142119.
36. Koskela, E., Mappes, T. & Ylönen, H. (1997) Territorial behaviour and reproductive success of bank vole Clethrionomys glareolus females. Journal of Animal Ecology, 66, 341-349.
37. Koskela, E., Mappes, T. & Ylönen, H. (1999) Experimental manipulation of breeding density and litter size: effects on reproductive success in the bank vole. Journal of Animal Ecology, 68, 513-521.
38. Lambin, X., Bretagnolle, V. & Yoccoz, N.G. (2006) Vole population cycles in northern and southern Europe: is there a need for different explanations for single pattern? Journal of Animal Ecology, 75, 340-349.
39. Luis, A.D., Douglass, R.J., Hudson, P.J., Mills, J.N. & Bjornstad, O.N. (2012) Sin Nombre hantavirus decreases survival of male deer mice. Oecologia, 169, 431-439.
40. Mappes, T. & Koskela, E. (2004) Genetic basis of the trade-off between offspring number and quality in the bank vole. Evolution, 58, 645-650.
41. Mappes, T. & Ylönen, H. (1997) Reproductive effort of bank vole females in a risky environment. Evolutionary Ecology, 11, 591-598.
42. Mappes, T., Grapputo, A., Hakkarainen, H., Huhta, E., Koskela, E., Saunanen, R. et al. (2008) Island selection on mammalian life histories: genetic differentiation in offspring size. BMC Evolutionary Biology, 8, 296.
43. Matthews, L. & Woolhouse, M. (2005) New approaches to quantifying the spread of infection. Nature Reviews Microbiology, 3, 529-536.
44. May, R.M. & Anderson, R.M. (1978) Regulation and stability of host-parasite population interactions: 2. Destabilizing processes. Journal of Animal Ecology, 47, 249-267.
45. Meyer, B.J. & Schmaljohn, C.S. (2000) Persistent hantavirus infections: characteristics and mechanisms. Trends in Microbiology, 8, 61-67.
46. Mills, J.N., Amman, B.R. & Glass, G.E. (2010) Ecology of hantaviruses and their hosts in North America. Vector-Borne and Zoonotic Diseases, 10, 563-574.
47. Mills, J.N. & Childs, J.E. (1998) Ecologic studies of rodent reservoirs: their relevance for human health. Emerging Infectious Diseases, 4, 529-537.
48. Niklasson, B., Hornfeldt, B., Lundkvist, A., Bjorsten, S. & Leduc, J. (1995) Temporal dynamics of Puumala virus antibody prevalence in voles and of nephropathia epidemica incidence in humans. American Journal of Tropical Medicine and Hygiene, 53, 134-140.
49. Oksanen, T.A., Koivula, M., Koskela, E. & Mappes, T. (2007) The cost of reproduction induced by body size at birth and breeding density. Evolution, 61, 2822-2831.
50. Olsson, G.E., Leirs, H. & Henttonen, H. (2010) Hantaviruses and their hosts in Europe: reservoirs here and there, but not everywhere? Vector-Borne and Zoonotic Diseases, 10, 549-561.
51. Olsson, G.E., White, N., Ahlm, C., Elgh, F., Verlemyr, A.C., Juto, P. et al. (2002) Demographic factors associated with hantavirus infection in bank voles (Clethrionomys glareolus). Emerging Infectious Diseases, 8, 924-929.
52. Olsson, G.E., Dalerum, F., Hornfeldt, B., Elgh, F., Palo, T.R., Juto, P. et al. (2003) Human hantavirus infections, Sweden. Emerging Infectious Diseases, 9, 1395-1401.
53. Ostfeld, R.S. & Holt, R.D. (2004) Are predators good for your health? Evaluating evidence for top-down regulation of zoonotic disease reservoirs. Frontiers in Ecology and the Environment, 2, 13-20.
54. Paterson, S. & Lello, J. (2003) Mixed models: getting the best use of parasitological data. Trends in Parasitology, 19, 370-375.
55. Prévot-Julliard, A.C., Henttonen, H., Yoccoz, N.G. & Stenseth, N.C.R. (1999) Delayed maturation in female bank voles: optimal decision or social constraint? Journal of Animal Ecology, 68, 684-697.
56. Schulte-Hostedde, A., Zinner, B., Millar, J.S. & Hickling, G.J. (2005) Restitution of mass-size residuals: validating body condition indices. Ecology, 86, 155-163.
57. Schwanz, L.E. (2008a) Offspring fitness: implications for adaptive reproductive strategies when parasitized. Functional Ecology, 22, 691-698.
58. Schwanz, L.E. (2008b) Chronic parasitic infection alters reproductive output in deer mice. Behavioral Ecology and Sociobiology, 62, 1351-1358.
59. Smith, M.J., White, A., Sherratt, J.A., Telfer, S., Begon, M. & Lambin, X. (2008) Disease effects on reproduction can cause population cycles in seasonal environments. Journal of Animal Ecology, 77, 378-389.
60. Soveri, T., Henttonen, H., Rudbäck, E., Schildt, R., Tanskanen, R., Husu-Kallio, J. et al. (2000) Disease patterns in field and bank vole populations during a cyclic decline in central Finland. Comparative Immunology, Microbiology & Infectious Diseases, 23, 73-89.
61. Staszewski, V., McCoy, K.D., Tveraa, T. & Boulinier, T. (2007) Interannual dynamics of antibody levels in naturally infected individuals of long-lived colonial birds. Ecology, 88, 3183-3191.
62. Stenseth, N.C. (1999) Population cycles in voles and lemmings: density dependence and phase dependence in a Stochastic World. Oikos, 87, 427-461.
63. Telfer, S., Bennett, M., Bown, K., Cavanagh, R., Crespin, L., Hazel, S. et al. (2002) The effects of cowpox virus on survival in natural rodent populations: increases and decreases. Journal of Animal Ecology, 71, 558-568.
64. Telfer, S., Bennett, M., Bown, K., Carslake, D., Cavanagh, R., Hazel, S. et al. (2005) Infection with cowpox virus decreases female maturation rates in wild populations of woodland rodents. Oikos, 109, 317-322.
65. Telfer, S., Birtles, R., Bennett, M., Lambin, X., Paterson, S. & Begon, M. (2008) Parasite interactions in natural populations: insights from longitudinal data. Parasitology, 135, 767-781.
66. Tersago, K., Verhagen, R. & Leirs, H. (2011) Temporal variation in individual factors associated with hantavirus infection in bank voles during an epizootic: implications for Puumala virus transmission dynamics. Vector-Borne and Zoonotic Diseases, 11, 715-721.
67. Tersago, K., Crespin, L., Verhagen, R. & Leirs, H. (2012) Impact of Puumala virus infection on maturation and survival in bank voles: a capture-mark-recapture analysis. Journal of Wildlife Diseases, 48, 148-156.
68. Tompkins, D.M. & Begon, M. (1999) Parasites can regulate wildlife populations. Parasitology Today, 15, 311-313.
69. Vapalahti, O., Kallio-Kokko, H., Närvänen, A., Julkunen, I., Lundkvist, Å., Plyusnin, A. et al. (1995) Human B-cell epitopes of Puumala virus nucleocapsid protein, the major antigen in early serological response. Journal of Medical Virology, 46, 293-303.
70. Vapalahti, O., Mustonen, J., Lundkvist, Å., Henttonen, H., Plyusnin, A. & Vaheri, A. (2003) Hantavirus infections in Europe. The Lancet Infectious Diseases, 3, 653-661.
71. Verhagen, R., Leirs, H., Tkachenko, E. & van der Groen, G. (1986) Ecological and epidemiological data on hantavirus in bank vole populations in Belgium. Archives of Virology, 91, 193-205.
72. Voutilainen, L. (2013) Interactions between Puumala hantavirus and its host, the bank vole, in the boreal zone. PhD thesis, University of Helsinki, Finland.
73. Voutilainen, L., Sironen, T., Tonteri, E., Tuiskunen Bäck, A., Razzauti, M., Karlsson, M. et al. (2015) Life-long shedding of Puumala hantavirus in wild bank vole (Myodes glareolus). Journal of General Virology. doi: 10.1099/vir.0.000076. [Epub ahead of print].
74. Woolhouse, M.E.J. & Gowtage-Sequaria, S. (2005) Host range and emerging and reemerging pathogens. Emerging Infectious Diseases, 11, 1842-1847.