• 1.

    Simone I, Provensal C, Polop J, 2012. Habitat use by corn mice (Calomys musculinus) in cropfield borders of agricultural ecosystems in Argentina. Wildl Res 39: 112122.

    • Search Google Scholar
    • Export Citation
  • 2.

    Mills JN, Ellis BA, McKee KT Jr., Calderon GE, Maiztegui JI, Nelson GO, Ksiazek TG, Peters CJ, Childs JE, 1992. A longitudinal study of Junín virus activity in the rodent reservoir of Argentine hemorrhagic fever. Am J Trop Med Hyg 47: 749763.

    • Search Google Scholar
    • Export Citation
  • 3.

    Sabattini MS, González de Ríos LE, Díaz G, Vega VR, 1977. Infección natural y experimental de roedores con virus Junín. Medicina (B Aires) 37: 149161.

    • Search Google Scholar
    • Export Citation
  • 4.

    Vitullo AD, Hodara VL, Merani MS, 1987. Effect of persistent infection with Junín virus on growth and reproduction of its natural reservoir, Calomys musculinus. Am J Trop Med Hyg 37: 663669.

    • Search Google Scholar
    • Export Citation
  • 5.

    Enria DA, Barrera Oro JG, 2002. Junín virus vaccines. Curr Top Microbiol Immunol 263: 239261.

  • 6.

    National Programme of Control of the Argentine Hemorrhagic Fever, 2015. Report of the XVIII Annual Meeting. Available at: http://www.anlis.gov.ar/inevh/?page_id=215. Accessed June 4, 2018.

  • 7.

    Mills JN, Ellis BA, McKee KT Jr., Ksiazek TG, Oro JG, Maiztegui JI, Calderon GE, Peters CJ, Childs JE, 1991. Junín virus activity in rodents from endemic and nonendemic loci in central Argentina. Am J Trop Med Hyg 44: 589597.

    • Search Google Scholar
    • Export Citation
  • 8.

    Polop J, Calderon G, Feuillade MR, García J, Enria D, Sabattini M, 2007. Spatial variation in abundance of the Junín virus hosts in endemic and nonendemic Argentine haemorrhagic fever zones. Austral Ecol 32: 245253.

    • Search Google Scholar
    • Export Citation
  • 9.

    Polop F, Provensal C, Scavuzzo M, Lamfri M, Calderon G, Polop J, 2008. On the relationship between the environmental history and the epidemiological situation of Argentine hemorrhagic fever. Ecol Res 23: 217225.

    • Search Google Scholar
    • Export Citation
  • 10.

    García JB, Morzunov SP, Levis S, Rowe J, Calderón G, Enría D, Sabattini M, Buchmeier MJ, Bowen MD, St. Jeor SC, 2000. Genetic diversity of the Junín virus in Argentina: geographic and temporal patterns. Virology 272: 127136.

    • Search Google Scholar
    • Export Citation
  • 11.

    Cross PC, Drewe J, Patrek V, Pearce G, Samuel MD, Delahay RJ, 2009. Wildlife population structure and parasite transmission: implications for disease management. Delahay RJ, Smith GC, Hutchings MR, eds. Management of Disease in Wild Mammals. Tokyo, Japan: Springer Japan, 9–29.

  • 12.

    Remais J, Akullian A, Ding L, Seto E, 2010. Analytical methods for quantifying environmental connectivity for the control and surveillance of infectious disease spread. J R Soc Interface 7: 11811193.

    • Search Google Scholar
    • Export Citation
  • 13.

    Barrett LG, Thrall PH, Burdon JJ, Linde CC, 2008. Life history determines genetic structure and evolutionary potential of host–parasite interactions. Trends Ecol Evol 23: 678685.

    • Search Google Scholar
    • Export Citation
  • 14.

    Biek R, Real LA, 2010. The landscape genetics of infectious disease emergence and spread. Mol Ecol 19: 35153531.

  • 15.

    Guivier E, Galan M, Chaval Y, Xuéreb A, Ribas Salvador A, Poulle ML, Voutilainen L, Henttonen H, Charbonnel N, Cosson JF, 2011. Landscape genetics highlights the role of bank vole metapopulation dynamics in the epidemiology of Puumala hantavirus. Mol Ecol 20: 35693583.

    • Search Google Scholar
    • Export Citation
  • 16.

    Mills JN, Ellis BA, Childs JE, McKee KT Jr., Maiztegui JI, Peters CJ, Ksiazek TG, Jahrling PB, 1994. Prevalence of infection with Junín virus in rodent populations in the epidemic area of Argentine hemorrhagic fever. Am J Trop Med Hyg 51: 554562.

    • Search Google Scholar
    • Export Citation
  • 17.

    Piacenza MF, 2012. Abundancia de Calomys musculinus, variables ambientales y diferencias en la incidencia de Fiebre Hemorrágica Argentina. PhD Thesis, Universidad Nacional de Río Cuarto, Cordoba, Argentina, 1–235.

  • 18.

    Gannon LW, Sikes RS; The Animal Care and Use Committee of the American Society of Mammalogists, 2007. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 88: 809823.

    • Search Google Scholar
    • Export Citation
  • 19.

    Mills JN, Yates TL, Childs JE, Parmenter RR, Ksiazek TG, Rollin PE, Peters CJ, 1995. Guidelines for working with rodents potentially infected with hantavirus. J Mammal 76: 716722.

    • Search Google Scholar
    • Export Citation
  • 20.

    Sikes RS, Gannon WL; Animal Care and Use Committee of the American Society of Mammalogists, 2011. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92: 235253.

    • Search Google Scholar
    • Export Citation
  • 21.

    Bruford ME, Hanotte O, Brookfield JFY, Burke T, 1992. Single-locus and multilocus DNA fingerprinting. Hoelzel AR, ed. Molecular Genetic Analysis of Populations, A Practical Approach. Oxford, United Kingdom: Oxford University Press, 225–269.

  • 22.

    Chiappero MB, Gardenal CN, Panzetta-Dutari GM, 2005. Isolation and characterization of microsatellite markers in Calomys musculinus (Muridae, Sigmodontinae, Phyllotini), the natural reservoir of Junín virus. Mol Ecol Notes 5: 593595.

    • Search Google Scholar
    • Export Citation
  • 23.

    Alberto F, 2009. MsatAllele 1.0: an R package to visualize the binning of microsatellite alleles. J Hered 100: 394397.

  • 24.

    van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P, 2004. Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4: 535538.

    • Search Google Scholar
    • Export Citation
  • 25.

    Queller DC, Goodnight KF, 1989. Estimating relatedness using genetic markers. Evolution 42: 258275.

  • 26.

    Goudet J, 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Updated from: Goudet J 1995: FSTAT (vers. 1.2): a computer program to calculate F-statistics. J Hered 86: 485486.

    • Search Google Scholar
    • Export Citation
  • 27.

    Nikolic N, Chevalet C, 2014. Detecting past changes of effective population size. Evol Appl 7: 663681.

  • 28.

    Schlötterer C, 2000. Evolutionary dynamics of microsatellite DNA. Chromosoma 109: 365371.

  • 29.

    Selkoe KA, Toonen RJ, 2006. Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9: 615629.

    • Search Google Scholar
    • Export Citation
  • 30.

    Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW, 2016. InfoStat Versión 2016. Córdoba, Argentina: Grupo InfoStat, FCA, Universidad Nacional de Córdoba. Available at: http://www.infostat.com.ar. Accessed October 2, 2017.

  • 31.

    Mills JN, Ellis BA, McKee KT, Maiztegui JI, Childs JE, 1991b. Habitat associations and relative densities of rodent populations in cultivated areas of central Argentina. J Mammal 72: 470479.

    • Search Google Scholar
    • Export Citation
  • 32.

    Chiappero MB, Gardenal CN, 2003. Restricted gene flow in Calomys musculinus (Rodentia, Muridae), the natural reservoir of Junín virus. J Hered 94: 490495.

    • Search Google Scholar
    • Export Citation
  • 33.

    González Ittig RG, Gardenal CN, 2004. Recent range expansion and low levels of contemporary gene flow in Calomys musculinus: its relationship with the emergence and spread of Argentine haemorrhagic fever. Heredity 93: 535541.

    • Search Google Scholar
    • Export Citation
  • 34.

    Calderón G, 2004. Desarrollo de Indicadores de Riesgo de Contraer la Fiebre Hemorrágica Argentina, por medio de Roedores que Actúan como Reservorio de los Arenavirus en Argentina. PhD Thesis, Universidad Nacional del Litoral, Santa Fe, Argentina, 1–267.

  • 35.

    Keesing F, Holt RD, Ostfeld RS, 2006. Effects of species diversity on disease risk. Ecol Lett 9: 485498.

  • 36.

    Enría DA, Mills JN, Flick R, Bowen MD, Bausch D, Shieh W-J, Peters CJ, 2006. Arenavirus infections. Guerrant N, Walker D, Weller P, eds. Tropical Infectious Diseases: Principles, Pathogens and Practice. Philadelphia, PA: Elsevier, 734–755.

  • 37.

    Vitullo AD, Merani MS, 1990. Vertical transmission of Junín virus in experimentally infected adult Calomys musculinus. Intervirology 31: 339344.

    • Search Google Scholar
    • Export Citation
  • 38.

    Kusumoto K, Saitoh T, 2008. Effects of cold stress on immune function in the grey-sided vole, Clethrionomys rufocanus. Mammal Study 33: 1118.

    • Search Google Scholar
    • Export Citation
  • 39.

    Kallio ER, Voutilainen L, Vapalahti O, Vaheri A, Henttonen H, Koskela E, Mappes T, 2007. Endemic hantavirus infection impairs the winter survival of its rodent host. Ecology 88: 19111916.

    • Search Google Scholar
    • Export Citation
  • 40.

    Kallio ER, Helle H, Koskela E, Mappes T, Vapalahti O, 2015. Age‐related effects of chronic hantavirus infection on female host fecundity. J Anim Ecol 84: 12641272.

    • Search Google Scholar
    • Export Citation
  • 41.

    Dearing MD, Previtali MA, Jones JD, Ely PW, Wood BA, 2009. Seasonal variation in Sin Nombre virus infections in deer mice: preliminary results. J Wildl Dis 45: 430436.

    • Search Google Scholar
    • Export Citation
  • 42.

    Luis AD, Douglass RJ, Hudson PJ, Mills JN, Bjørnstad ON, 2012. Sin Nombre hantavirus decreases survival of male deer mice. Oecologia 169: 431439.

  • 43.

    Sommaro L, Gomez D, Bonatto F, Steinmann A, Chiappero M, Priotto J, 2010. Corn mice (Calomys musculinus) movement in linear habitats of agricultural ecosystems. J Mammal 91: 668673.

    • Search Google Scholar
    • Export Citation
  • 44.

    Vitullo AD, Merani MS, 1988. Is vertical transmission sufficient to maintain Junín virus in nature? J Gen Virol 69: 14371440.

 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

 

 

Effective Population Size Differences in Calomys musculinus, the Host of Junín Virus: Their Relationship with the Epidemiological History of Argentine Hemorrhagic Fever

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  • 1 Cátedra de Genética de Poblaciones y Evolución, Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de Córdoba, Córdoba, Argentina;
  • | 2 Instituto de Diversidad y Ecología Animal (IDEA), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Córdoba, Argentina;
  • | 3 Departamento de Ciencias Naturales, Universidad Nacional de Río Cuarto, Río Cuarto, Argentina;
  • | 4 Instituto Nacional de Enfermedades Virales Humanas, “Dr. Julio I. Maiztegui”, Pergamino, Argentina
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Argentine hemorrhagic fever (AHF) is a serious endemic disease in Argentina, produced by Junín virus, whose host is the Sigmodontinae rodent Calomys musculinus. Within the endemic area, human incidence and proportion of infected rodents remains high for 5–10 years after the first appearance of the disease (epidemic [E] zone) and then gradually declines to sporadic cases (historic [H] zone). We tested the hypothesis that host populations within the E zone are large and well connected by gene flow, facilitating the transmission and maintenance of the virus, whereas those in the H and nonendemic (NE) zones are small and isolated, with the opposite effect. We estimated parameters affected by levels of gene flow and population size in 14 populations of C. musculinus: population effective size (Ne), genetic variability, and mean relatedness. Our hypothesis was not supported: the lowest levels of variability and of Ne and the highest genetic relatedness among individuals were found in the H zone. Populations from the NE zone displayed opposite results, whereas those in the E zone showed intermediate values. If we consider that populations are first NE, then E, and finally H, a correlative decrease in Ne was observed. Chronically infected females have a low reproductive success. We propose that this would lower Ne because each cohort would originate from a fraction of females of the previous generation, and affect other factors such as proportion of individuals that develop acute infection, probability of viral transmission, and evolution of virulence, which would explain, at least partly, the changing incidence of AHF.

Author Notes

Address correspondence to Marina B. Chiappero, Cátedra de Genética de Poblaciones y Evolución, Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de Córdoba, Avenida Vélez Sarsfield 299, Córdoba 5000, Argentina. E-mail: marina.chiappero@unc.edu.ar

Financial support: This research was supported by the Fondo para la Investigación Científica y Tecnológica of Argentina (FONCyT; Grant number PICT0458/08).

Authors’ addresses: Marina B. Chiappero and Cristina N. Gardenal, Cátedra de Genética de Poblaciones y Evolución, Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de Córdoba, Córdoba, Argentina, and Instituto de Diversidad y Ecología Animal (IDEA), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Córdoba, Argentina, E-mails: marina.chiappero@unc.edu.ar and ngardenal@unc.edu.ar. María Florencia Piacenza, María Cecilia Provensal, and Jaime J. Polop, Departamento de Ciencias Naturales, Universidad Nacional de Río Cuarto, Río Cuarto, Argentina, E-mails: fpiacenza@exa.unrc.edu.ar, cprovensal@exa.unrc.edu.ar, and jpolop@exa.unrc.edu.ar. Gladys E. Calderón, Instituto Nacional de Enfermedades Virales Humanas, “Dr. Julio I. Maiztegui”, Pergamino, Argentina, E-mail: gcalderon@anlis.gov.ar.

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