Abstract
Hantaviruses are among the main emerging infectious agents in Europe. Their mode of transmission in natura is still not well known. In particular, social features and behaviours could be crucial for understanding the persistence and the spread of hantaviruses in rodent populations. Here, we investigated the importance of kinclustering and dispersal in hantavirus transmission by combining a fine-scale spatiotemporal survey (4 km2) and a population genetics approach. Two specific host-hantavirus systems were identified and monitored: the bank vole Myodes, earlier Clethrionomys glareolus––Puumala virus and the common vole Microtus arvalis—Tula virus. Sex, age and landscape characteristics significantly influenced the spatial distribution of infections in voles. The absence of temporal stability in the spatial distributions of viruses suggested that dispersal is likely to play a role in virus propagation. Analysing vole kinship from microsatellite markers, we found that infected voles were more closely related to each other than non-infected ones. Winter kin-clustering, shared colonies within matrilineages or delayed dispersal could explain this pattern. These two last results hold, whatever the host-hantavirus system considered. This supports the roles of relatedness and dispersal as general features for hantavirus transmission.
Similar content being viewed by others
References
Barker FS, Helyar SJ, Kemp SJ, Begon M (2005) Highly polymorphic microsatellite loci in the bank vole (Clethrionomys glareolus). Mol Ecol Notes 5:311–313
Bernshtein AD, Apekina NS, Mikhailova TV, Myasnikov YA, Khlyap LA, Korotkov YS, Gabrilovskaya IN (1999) Dynamics of Puumala hantavirus infection in naturally infected bank voles (Clethrionomys glareolus). Arch Virol 144:2415–2428
Berthier K, Charbonnel N, Galan M, Chaval Y, Cosson J-F (2006) Migration and recovery of the genetic diversity during the increasing density phase in cyclic vole populations. Mol Ecol 15:2665–2676
Boonstra R, Krebs CJ, Gaines MS, Johnson ML, Craine ITM (1987) Natal philopatry and breeding systems in voles (Microtus spp.). J Anim Ecol 56:655–673
Botten J, Mirowsky K, Ye CY, 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
Boyce CCK, Boyce JL (1988) Population biology of Microtus arvalis. I. Lifetime reproductive success of solitary and grouped breeding females. J Anim Ecol 57:711–722
Boyce CCK, Boyce JL (1988) Population biology of Microtus arvalis. III. Regulation of numbers and breeding dispersion of females. J Anim Ecol 57:737–754
Bujalska G (1988) Lihe history consequences of territoriality in the bank vole. In: Boyce MS (ed) Evolution of life histories: theories and patters from mammals. Yale University Press, Edmonton, pp 75–90
Bujalska G (1990) Social system of the bank vole Clethrionomys glareolus. In: Tamarin R, Ostfeld R, Pugh S, Bujalska G (eds) Social system and population cycles in Voles ALS-Verlag, Birkhauser, Basel, pp 155–167
Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach. Springer, New York
Davis S, Calvet E, Leirs H (2005) Fluctuating rodent populations and risk to humans from rodent-borne zoonoses. Vector Borne Zoonotic Dis 5:305–314
Deter J, Bryja J, Chaval Y, Galan M, Henttonen H, Laakkonen J, Voutilainen L, Vapalahti O, Vaheri A, Ribas Salvadore A, Morand S, Cosson J-F, Charbonnel N (2007) Association between the DQA MHC class II gene and Puumala virus infection in Myodes glareolus, the bank vole. Inf Genet Evol (in press)
Dobly A (2001) Movement patterns of male common voles (Microtus arvalis) in a network of Y junctions: role of distant visual cues and scent marks. Can J Zool 79:2228–2238
Dohmae K, Nishimuney Y (1995) Protection against hantavirus infection by dams immunity transferred vertically to neonates. Arch Virol 140:165–172
Escutenaire S, Chalon P, Verhagen R, Heyman P, Thomas I, Karelle-Bui L, Avsic-Zupanc T, Lundkvist Å, Plyusnin A, Pastoret P-P (2000) Spatial and temporal dynamics of Puumala hantavirus infection in red bank vole (Clethrionomys glareolus) populations in Belgium. Virus Res 67:91–107
Escutenaire S, Chalon P, De Jaegere F, Karelle-Bui L, Mees G, Brochier B, Rozenfeld F, Pastoret PP (2002) Behavioral, physiologic, and habitat influences on the dynamics of Puumala virus infection in bank voles (Clethrionomys glareolus). Emerg Infect Dis 8:930–936
Gauffre B, Galan M, Bretagnolle V, Cosson J-F (2007) Polymorphic microsatellite loci and PCR multiplexing in the common vole, Microtus arvalis. Mol Ecol Notes 7:830–832
Giraudoux P, Pradier B, Delattre P, Deblay S, Salvi D, Defaut R (1995) Estimation of water vole abundance by using surface indices. Acta Theriol 40:77–96
Gockel J, Harr B, Schlotterer C, Arnold W, Gerlach G, Tautz D (1997) Isolation and characterization of microsatellite loci from Apodemus flavicollis (Rodentia, Muridae) and Clethrionomys glareolus (Rodentia, Cricetidae). Mol Ecol 6:597–599
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Heyman P, Plyusnina A, Berny P, Cochez C, Artois M, Zizi M, Pirnay JP, Plyusnin A (2004) Seoul hantavirus in Europe: first demonstration of the virus genome in wild R. norvegicus captured in France. Eur J Clin Microbiol Infect Dis 23:711–717
Innes DGL, Millar JS (1994) Life-histories of Clethrionomys and Microtus (Microtinae). Mamm Rev 24:179–207
Ishibashi Y, Saitoh T, Abe S, Yoshida MC (1997) Cross species amplification of microsatellite DNA in Old World microtine rodents with PCR primers for the gray-sided vole, Clethrionomys rufocanus. Mammal Study 22:5–10
Ishibashi Y, Saitoh T, Abe S, Yoshida MC (1998) Kin-related social organization in a winter population of the vole Clethrionomys rufocanus. Res Popul Ecol 40:51–59
Ishibashi Y, Yoshinaga Y, Saitoh T, Abe S, Iida H, Yoshida MC (1999) Polymorphic microsatellite DNA markers in the field vole Microtus montebelli. Mol Ecol 8:163–164
IVS IdVS (2005) Recrudescence des infections à Hantavirus, Nord-Est de la France. Point au http://www.invssantefr/presse/2005/le_point_sur/hantavirus_121005/indexhtml (Accessed 12 October 2005)
Iwasa MA, Kariwa H, Cui B-Z, Lokugamage K, Lokugamage N, Hagiya T, Mizutani T, Takashima I (2004) Modes of hantavirus transmission in a population of Clethrionomys rufocanus bedfordiae inferred from mitochondrial and microsatellite DNA analyses. Arch Virol 149:929–941
Jánová E, Heroldová M, Nesvadbová J, Bryja J, Tkadlec E (2003) Age variation in a fluctuating population of the common vole. Oecologia 137:527–532
Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108
Kallio-Kokko H, Laakkonen J, Rizzoli A, Tagliapietra V, Cattadori I, Perkins SE, Hudson PJ, Cristofolini A, Versini W, Vapalahti O, Vaheri A, Henttonen H (2006) Hantavirus and arenavirus antibody prevalence in rodents and humans in Trentino, Northern Italy. Epidemiol Infect 134:830–836
Kallio ER, Klingström J, Gustafsson E, Manni T, Vaheri A, Henttonen H, Vapalahti O, Lundkvist A (2006) Prolonged survival of Puumala hanatvirus outside the host: evidence for indirect transmission via the environment. J Gen Virol 87:2127–2134
Kallio ER, Poikonen A, Vaheri A, Vapalahti O, Henttonen H, Koskela E, Mappes T (2006) Maternal antibodies postpone hantavirus infection and enhance individual breeding success. Proc R Soc B Biol Sci 273:2771–2776
Khlyap LA, Albov SA, Serbenyuk MA, Zagarujko NV (1989) Ecologo-ethological preconditions of infections transmission among bank voles by theirs excreta. In: XII All-Union
Klein S (2005) Host factors mediating sex differences in viral infection. Gend Med 2:197–207
Klein SL, Cernetich A, Hilmer S, Hoffman EP, Scott AL, Glass GE (2004) Differential expression of immunoregulatory genes in male and female Norway rats following infection with Seoul virus. J Med Virol 74:180–190
Klein SL, Zink MC, Glass GE (2004) Seoul virus infection increases aggressive behaviour in male Norway rats. Anim Behav 67:421–429
Klingstrom J, Heyman P, Escutenaire S, Sjolander KB, De Jaegere F, Henttonen H, Lundkvist A (2002) Rodent host specificity of European hantaviruses: evidence of Puumala virus interspecific spillover. J Med Virol 68:581–588
Li CC, Weeks DE, Chakravarti A (1993) Similarity of DNA finger-prints due to chance and relatedness. Heredity 43:45–52
Martinet L (1966) Détermination de l’âge chez le campagnol des champs (Microtus arvalis) par la pesée du cristallin. Mammalia 30:425–430
McCaughey C, Hart CA (2000) Hantaviruses. J Med Microbiol 49:587–599
McCullagh P, Nelder J (1989) Generalized linear models. Chapman and Hall, New York
Michaux JR, Kinet S, Filippucci M-G, Libois R, Besnard A, Catzeflis F (2001) Molecular identification of three sympatric species of wood mice (Apodemus sylvaticus, A. flavicollis, A. alpicola) in western Europe (Muridae: Rodentia). Mol Ecol Notes 1:260–263
Mills JN, Childs J, Ksiazek TG, Peters CJ, Velleca WM (1995) Methods for trapping and sampling small mammals for virologic testing. Centers for Disease Control and Prevention, Atlanta
Miyamoto H, Kariwa H, Araki K, Lokugamage K, Hayasaka D, Cui BZ, Lokugamage N, Ivanov LI, Mizutani T, Iwasa MA, Yoshimatsu K, Arikawa J, Takashima I (2003) Serological analysis of hemorrhagic fever with renal syndrome (HFRS) patients in far eastern Russia and identification of the causative hantavirus genotype. Arch Virol 148:1543–1556
Nelson RJ, Demas GE, Klein SL, Kriegsfeld LJ (eds) (2002) Seasonal patterns of stress, immune function, and disease, Cambridge University Press, Cambridge
Olsson GE, White N, Ahlm C, Elgh F, Verlemyr AC, Juto P, Palo RT (2002) Demographic factors associated with hantavirus infection in bank voles (Clethrionomys glareolus). Emerg Infect Dis 8:924–929
Olsson GE (2003) Nephropathia Epidemica and Puumala virus occurrence in relation to bank vole (Clethrionomys glareolus) dynamics and environmental factors in Northern Sweden. Swedish University of Agricultural Sciences, Umeå
Olsson GE, White N, Hjältén J, Ahlm C (2005) Habitat factors associated with bank voles (Clethrionomys glareolus) and concomitant hantavirus in northern Sweden. Vector Borne Zoonotic Dis 5:315–323
Paetkau D, Slade R, Burden M, Estoup A (2004) Direct, real-time estimation of migration rate using assignment methods: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65
Penalba C, Galempoix JM, Lanoux P (2001) Epidémiologie des infections à hantavirus en France. Médecine et Maladie Infectieuses 31(Suppl 2):272–284
Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) Geneclass2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539
Plyusnin A (2002) Genetics of hantaviruses: implications to taxonomy. Arch Virol 147:665–682
Plyusnina A, Deter J, Charbonnel N, Cosson J-F, Plyusnin A (2007) Puumala and Tula hantaviruses in France. Virus Res (in press)
Prévot-Julliard A-C, Henttonen H, Yoccoz NG, Stenseth NC (1999) Delayed maturation in female bank voles: optimal decision or social constraint? J Anim Ecol 68:684–697
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenism. J Hered 86:248–249
Rosà R, Rizzoli A, Ferrari N, Pugliese A (2006) Models for host–macroparasite interactions in micromammals. In: Morand S, Krasnov BR, Poulin R (eds) Micromammals and macroparasites from evolutionary study to management. Springer, Tokyo, pp 319–348
Sauvage F, Langlais M, Yoccoz NG, Pontier D (2003) Modelling hantavirus in fluctuating populations of bank voles: the role of indirect transmission on virus persistence. J Anim Ecol 72:1–13
Sauvage F (2004) La synergie entre dynamique des populations réservoirs de campagnols roussâtres et excrétion du hantavirus Puumala : mise en évidence du mécanisme d’émergence de la néphropathie épidémique humaine Lyon. Université Claude Bernard––Lyon 1, Lyon, p 225
Schultze D, Lundkvist A, Blauenstein U, Heyman P (2002) Tula virus infection associated with fever and exanthema after a wild rodent bite. Eur J Clin Microbiol Infect Dis 21:304–306
Somsook S, Steiner HM (1991) Zur grosse des Aktionraumes von Microtus arvalis (Pallas, 1779). Z Saugetierkd 56:200–206
Spitz F (1974) Démographie du campagnol des champs Microtus arvalis en vendée. Annales de Zoologie - Ecologie Animale 6:259–312
Spitz F, Le Louarn H, Poulet A, Dassonville B (1974) Standardisation des piégeages en ligne pour quelques espèces de rongeurs. Revue d’Ecologie (Terre et Vie) 28:564–578
Stewart WA, Piertney SB, Dallas JF (1998) Isolation and characterization of highly polymorphic microsatellites in the water vole, Arvicola terrestris. Mol Ecol 7:1258–1259
Vapalahti O, Mustonen J, Lundkvist A, Henttonen H, Plyusnin A, Vaheri A (2003) Hantavirus infections in Europe. Lancet Infect Dis 3:753–754
Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935
Verhagen R, Leirs H, Verheyen W (2000) Demography of Cletrionomys glareolus, Belgium. Pol J Ecol 48:113–123
Wang J (2002) An estimator for pairwise relatedness using molecular markers. Genetics 160:1203–1215
Weir BS, Cockerman CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Wolff JO, Sherman PW (2007) Rodent Societies: An Ecological and Evolutionary Perspective. University Press, Chicago
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle River
Zeier M, Handermann M, Bahr U, Rensch B, Muller S, Kehm R, Muranyi W, Darai G (2005) New ecological aspects of hantavirus infection: a change of a paradigm and a challenge of prevention––a review. Virus Genes 30:157–180
Acknowledgments
We thank Sylvain Piry, Florian Holon, Audrey Scala and Josef Bryja for assistance with the field work. We are very grateful to Valérie Deffontaine for lending microsatellites primers and the protocol for the bank vole. We also thank Johan Michaux for lending primers for Apodemus identification. This work was financed by a grant from the Ministry of Research and supported financially by the Institut National de la Recherche Agronomique, the region Franche-Comté and the DIREN Franche-Comté. Our work was also partially funded by EU grant GOCE-2003-010284 EDEN and is catalogued by the EDEN Steering Committee as EDEN0069 (http://www.eden-fp6project.net).
Author information
Authors and Affiliations
Corresponding author
Additional information
N. Charbonnel and J.-F. Cosson have contributed equally.
Rights and permissions
About this article
Cite this article
Deter, J., Chaval, Y., Galan, M. et al. Kinship, dispersal and hantavirus transmission in bank and common voles. Arch Virol 153, 435–444 (2008). https://doi.org/10.1007/s00705-007-0005-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-007-0005-6