When Viruses Don't Go Viral: The Importance of Host Phylogeographic Structure in the Spatial Spread of Arenaviruses

. 2017 Jan ; 13 (1) : e1006073. [epub] 20170111

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid28076397
Odkazy

PubMed 28076397
PubMed Central PMC5226678
DOI 10.1371/journal.ppat.1006073
PII: PPATHOGENS-D-16-01576
Knihovny.cz E-zdroje

Many emerging infections are RNA virus spillovers from animal reservoirs. Reservoir identification is necessary for predicting the geographic extent of infection risk, but rarely are taxonomic levels below the animal species considered as reservoir, and only key circumstances in nature and methodology allow intrinsic virus-host associations to be distinguished from simple geographic (co-)isolation. We sampled and genetically characterized in detail a contact zone of two subtaxa of the rodent Mastomys natalensis in Tanzania. We find two distinct arenaviruses, Gairo and Morogoro virus, each spatially confined to a single M. natalensis subtaxon, only co-occurring at the contact zone's centre. Inter-subtaxon hybridization at this centre and a continuum of quality habitat for M. natalensis show that both viruses have the ecological opportunity to spread into the other substaxon's range, but do not, strongly suggesting host-intrinsic barriers. Such barriers could explain why human cases of another M. natalensis-borne arenavirus, Lassa virus, are limited to West Africa.

Zobrazit více v PubMed

Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, et al. Global trends in emerging infectious diseases. Nature. 2008;451(7181):990–3. Epub 2008/02/22. 10.1038/nature06536 PubMed DOI PMC

Drosten C. Virus ecology: a gap between detection and prediction. Emerg Microbes Infect. 2013;2(5):e31 10.1038/emi.2013.25 PubMed DOI PMC

Baize S, Pannetier D, Oestereich L, Rieger T, Koivogui L, Magassouba N, et al. Emergence of Zaire Ebola virus disease in Guinea. New Engl J Med. 2014;371(15):1418–25. 10.1056/NEJMoa1404505 PubMed DOI

Monroe MC, Morzunov SP, Johnson AM, Bowen MD, Artsob H, Yates T, et al. Genetic diversity and distribution of Peromyscus-borne hantaviruses in North America. Emerg Infect Dis. 1999;5(1):75–86. 10.3201/eid0501.990109 PubMed DOI PMC

Morzunov SP, Rowe JE, Ksiazek TG, Peters CJ, St Jeor SC, Nichol ST. Genetic analysis of the diversity and origin of hantaviruses in Peromyscus leucopus mice in North America. J Virol. 1998;72(1):57–64.PubMed Central PMCID: PMC109349. PubMed PMC

Drebot MA, Gavrilovskaya I, Mackow ER, Chen Z, Lindsay R, Sanchez AJ, et al. Genetic and serotypic characterization of Sin Nombre-like viruses in Canadian Peromyscus maniculatus mice. Virus Res. 2001;75(1):75–86. PubMed

Dragoo JW, Lackey JA, Moore KE, Lessa EP, Cook JA, Yates TL. Phylogeography of the deer mouse (Peromyscus maniculatus) provides a predictive framework for research on hantaviruses. J Gen Virol. 2006;87:1997–2003. 10.1099/vir.0.81576-0 PubMed DOI

González-Ittig RE, Salazar-Bravo J, Barquez RM, Gardenal CN. Phylogenetic relationships among species of the genus Oligoryzomys (Rodentia, Cricetidae) from Central and South America. Zoologica Scripta. 2010;39(6):511–26.

Gonder MK, Locatelli S, Ghobrial L, Mitchell MW, Kujawski JT, Lankester FJ, et al. Evidence from Cameroon reveals differences in the genetic structure and histories of chimpanzee populations. Proc Natl Acad Sci USA. 2011;108(12):4766–71. 10.1073/pnas.1015422108 PubMed DOI PMC

Keele BF, Van Heuverswyn F, Li Y, Bailes E, Takehisa J, Santiago ML, et al. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science. 2006;313(5786):523–6. 10.1126/science.1126531 PubMed DOI PMC

Li Y, Ndjango JB, Learn GH, Ramirez MA, Keele BF, Bibollet-Ruche F, et al. Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir. J Virol. 2012;86(19):10776–91. Epub 2012/07/28. PubMed Central PMCID: PMCPMC3457319. 10.1128/JVI.01498-12 PubMed DOI PMC

Liu W, Worobey M, Li Y, Keele BF, Bibollet-Ruche F, Guo Y, et al. Molecular ecology and natural history of simian foamy virus infection in wild-living chimpanzees. PLoS Pathog. 2008;4(7):e1000097 10.1371/journal.ppat.1000097 PubMed DOI PMC

Goyens J, Reijniers J, Borremans B, Leirs H. Density thresholds for Mopeia virus invasion and persistence in its host Mastomys natalensis. Journal of theoretical biology. 2013;317:55–61. 10.1016/j.jtbi.2012.09.039 PubMed DOI

Lloyd-Smith JO, Cross PC, Briggs CJ, Daugherty M, Getz WM, Latto J, et al. Should we expect population thresholds for wildlife disease? Trends in Ecology & Evolution. 2005;20(9):511–9. PubMed

Hewitt GM. Speciation, hybrid zones and phylogeography—or seeing genes in space and time. Mol Ecol. 2001;10(3):537–49. PubMed

Hewitt G. The genetic legacy of the Quaternary ice ages. Nature. 2000;405(6789):907–13. 10.1038/35016000 PubMed DOI

Barton NH, Hewitt GM. Analysis of Hybrid Zones. Annual Review of Ecology, Evolution, and Systematics. 1985;16:113–48.

Goüy de Bellocq J, Baird SJE, Albrechtova J, Sobekova K, Pialek J. Murine cytomegalovirus is not restricted to the house mouse Mus musculus domesticus: prevalence and genetic diversity in the European house mouse hybrid zone. J Virol. 2015;89(1):406–14. PubMed Central PMCID: PMC4301121. 10.1128/JVI.02466-14 PubMed DOI PMC

Kváč M, McEvoy J, Loudová M, Stenger B, Sak B, Květoňová D, et al. Coevolution of Cryptosporidium tyzzeri and the house mouse (Mus musculus). Int J Parasitol. 2013;43(10):805–17. 10.1016/j.ijpara.2013.04.007 PubMed DOI PMC

Charleston MA, Robertson DL. Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny. Syst Biol. 2002;51(3):528–35. 10.1080/10635150290069940 PubMed DOI

Ramsden C, Holmes EC, Charleston MA. Hantavirus evolution in relation to its rodent and insectivore hosts: no evidence for codivergence. Mol Biol Evol. 2009;26(1):143–53. Epub 2008/10/17. 10.1093/molbev/msn234 PubMed DOI

Jackson AP, Charleston MA. A cophylogenetic perspective of RNA-virus evolution. Mol Biol Evol. 2004;21(1):45–57. Epub 2003/09/02. 10.1093/molbev/msg232 PubMed DOI

Holmes EC. Error thresholds and the constraints to RNA virus evolution. Trends Microbiol. 2003;11:543–6. PubMed PMC

Faria NR, Suchard MA, Rambaut A, Streicker DG, Lemey P. Simultaneously reconstructing viral cross-species transmission history and identifying the underlying constraints. Philos T R Soc B. 2013;368(1614). Artn 20120196 PubMed PMC

Streicker DG, Turmelle AS, Vonhof MJ, Kuzmin IV, McCracken GF, Rupprecht CE. Host phylogeny constrains cross-species emergence and establishment of rabies virus in bats. Science. 2010;329(5992):676–9. 10.1126/science.1188836 PubMed DOI

Longdon B, Hadfield JD, Webster CL, Obbard DJ, Jiggins FM. Host phylogeny determines viral persistence and replication in novel hosts. PLoS Pathog. 2011;7(9). Artn E1002260 PubMed PMC

Iacono GL, Cunningham AA, Fichet-Calvet E, Garry RF, Grant DS, Khan SH, et al. Using modelling to disentangle the relative contributions of zoonotic and anthroponotic transmission: the case of Lassa fever. PLoS Negl Trop Dis. 2015;9(1):e3398 10.1371/journal.pntd.0003398 PubMed DOI PMC

Andersen KG, Shapiro BJ, Matranga CB, Sealfon R, Lin AE, Moses LM, et al. Clinical Sequencing Uncovers Origins and Evolution of Lassa Virus. Cell. 2015;162(4):738–50. PubMed Central PMCID: PMCPMC4537774. 10.1016/j.cell.2015.07.020 PubMed DOI PMC

WHO. Lassa fever. Fact Sheet 2005;179:1–2.

Bausch DG, Mills JN. Arenaviruses: Lassa Fever, Lujo Hemorrhagic Fever, Lymphocytic Choriomeningitis, and the South American Hemorrhagic Fevers In: Kaslow RA, Stanberry LR, Le Duc JW, editors. Viral Infections of Humans: Springer US; 2014. p. 147–71.

Lecompte E, Fichet-Calvet E, Daffis S, Koulémou K, Sylla O, Kourouma F, et al. Mastomys natalensis and Lassa fever, West Africa. Emerg Infect Dis. 2006;12(12):1971 10.3201/eid1212.060812 PubMed DOI PMC

Safronetz D, Sogoba N, Lopez JE, Maiga O, Dahlstrom E, Zivcec M, et al. Geographic distribution and genetic characterization of Lassa Virus in Sub-Saharan Mali. PLoS Negl Trop Dis. 2013;7(12):e2582 10.1371/journal.pntd.0002582 PubMed DOI PMC

Leski TA, Stockelman MG, Moses LM, Park M, Stenger DA, Ansumana R, et al. Sequence variability and geographic distribution of Lassa virus, Sierra Leone. Emerg Infect Dis. 2015;21(4):609–18. 10.3201/eid2104.141469 PubMed DOI PMC

Olayemi A, Cadar D, Magassouba N, Obadare A, Kourouma F, Oyeyiola A, et al. New Hosts of The Lassa Virus. Sci Rep. 2016;6:25280 PubMed Central PMCID: PMCPMC4853722. 10.1038/srep25280 PubMed DOI PMC

Wulff H, McIntosh BM, Hamner DB, Johnson K. Isolation of an arenavirus closely related to Lassa virus from Mastomys natalensis in south-east Africa. Bull WHO. 1977;55:441–4. PubMed PMC

Günther S, Hoofd G, Charrel R, Roser C, Becker-Ziaja B, Lloyd G, et al. Mopeia virus-related arenavirus in Natal multimammate mice, Morogoro, Tanzania. Emerg Infect Dis. 2009;15(12):2008–12. Epub 2009/12/08. PubMed Central PMCID: PMC3044542. 10.3201/eid1512.090864 PubMed DOI PMC

Ishii A, Thomas Y, Moonga L, Nakamura I, Ohnuma A, Hang'ombe B, et al. Novel arenavirus, Zambia. Emerg Infect Dis. 2011;17(10):1921 PubMed Central PMCID: PMC3310648. 10.3201/eid1710.101452 PubMed DOI PMC

Gryseels S, Rieger T, Oestereich L, Cuypers B, Borremans B, Makundi R, et al. Gairo virus, a novel arenavirus of the widespread Mastomys natalensis: Genetically divergent, but ecologically similar to Lassa and Morogoro viruses. Virology. 2015;476:249–56. 10.1016/j.virol.2014.12.011 PubMed DOI

Olayemi A, Obadare A, Oyeyiola A, Igbokwe J, Fasogbon A, Igbahenah F, et al. Arenavirus Diversity and Phylogeography of Mastomys natalensis Rodents, Nigeria. Emerg Infect Dis. 2016;22(4):687–90. PubMed Central PMCID: PMCPMC4806935. PubMed PMC

Safronetz D, Lopez JE, Sogoba N, Traoré SF, Raffel SJ, Fischer ER, et al. Detection of Lassa virus, Mali. Emerg Infect Dis. 2010;16(7):1123–6. 10.3201/eid1607.100146 PubMed DOI PMC

Fichet-Calvet E, Rogers DJ. Risk maps of Lassa fever in West Africa. PLoS Negl Trop Dis. 2009;3(3):e388 Epub 2009/03/04. PubMed Central PMCID: PMC2644764. 10.1371/journal.pntd.0000388 PubMed DOI PMC

Ehichioya DU, Hass M, Becker-Ziaja B, Ehimuan J, Asogun DA, Fichet-Calvet E, et al. Current molecular epidemiology of Lassa virus in Nigeria. J Clin Microbiol. 2011;49(3):1157–61. Epub 2010/12/31. PubMed Central PMCID: PMC3067713. 10.1128/JCM.01891-10 PubMed DOI PMC

Colangelo P, Verheyen E, Leirs H, Tatard C, Denys C, Dobigny G, et al. A mitochondrial phylogeographic scenario for the most widespread African rodent, Mastomys natalensis. Biol J Linn Soc. 2013;108(4):901–16.

Bryja J, Mazoch V, Patzenhauerova H, Mateke C, Zima J, Skliba J, et al. Revised occurrence of rodents from the tribe Praomyini (Muridae) in Zambia based on mitochondrial DNA analyses: implications for biogeography and conservation. Folia Zool. 2012;61(3–4):268–83.

Ishii A, Thomas Y, Moonga L, Nakamura I, Ohnuma A, Hang'ombe BM, et al. Molecular surveillance and phylogenetic analysis of Old World arenaviruses in Zambia. J Gen Virol. 2012;93:2247–51. 10.1099/vir.0.044099-0 PubMed DOI

Goüy de Bellocq J, Borremans B, Katakweba A, Makundi R, Baird SJE, Becker-Ziaja B, et al. Sympatric occurrence of 3 arenaviruses, Tanzania. Emerg Infect Dis. 2010;16(4):692–5. Epub 2010/03/31. 10.3201/eid1604.091721 PubMed DOI PMC

Lecompte E, Ter Meulen J, Emonet S, Daffis S, Charrel R. Genetic identification of Kodoko virus, a novel arenavirus of the African pigmy mouse (Mus Nannomys minutoides) in West Africa. Virology. 2007;364(1):178–83. 10.1016/j.virol.2007.02.008 PubMed DOI

Coulibaly-N'Golo D, Allali B, Kouassi SK, Fichet-Calvet E, Becker-Ziaja B, Rieger T, et al. Novel arenavirus sequences in Hylomyscus sp. and Mus (Nannomys) setulosus from Cote d'Ivoire: implications for evolution of arenaviruses in Africa. PLoS One. 2011;6(6). PubMed PMC

Swanepoel R, Leman PA, Shepherd AJ, Shepherd SP, Kiley MP, McCormick JB. Identification of Ippy as a Lassa-fever-related virus. The Lancet. 1985;325(8429):639. PubMed

Fulhorst CF, Milazzo ML, Carroll DS, Charrel RN, Bradley RD. Natural host relationships and genetic diversity of Whitewater Arroyo virus in southern Texas. Am J Trop Med Hyg. 2002;67(1):114–8. PubMed

Lavergne A, De Thoisy B, Donato D, Guidez A, Matheus S, Catzeflis F, et al. Patawa Virus, a new arenavirus hosted by forest rodents in French Guiana. EcoHealth. 2014:1–8. PubMed

Li K, Lin XD, Wang W, Shi M, Guo WP, Zhang XH, et al. Isolation and characterization of a novel arenavirus harbored by rodents and shrews in Zhejiang province, China. Virology. 2015;476:37–42. 10.1016/j.virol.2014.11.026 PubMed DOI

Blasdell KR, Duong V, Eloit M, Chretien F, Ly S, Hul V, et al. Evidence of human infection by a new mammarenavirus endemic to Southeastern Asia. Elife. 2016;5. PubMed Central PMCID: PMCPMC4900801. PubMed PMC

Leirs H. Mastomys In: Kingdon Jonathan, Happold David, Butynski Thomas, Hoffmann Michael, Happold Meredith, Kalina J, editors. Mammals of Africa: Volume III. 3 1st ed ed. London, UK: Bloomsbury Publishing; 2013. p. 460–72.

Mylne AQ, Pigott DM, Longbottom J, Shearer F, Duda KA, Messina JP, et al. Mapping the zoonotic niche of Lassa fever in Africa. Trans R Soc Trop Med Hyg. 2015;109(8):483–92. PubMed Central PMCID: PMC4501400. 10.1093/trstmh/trv047 PubMed DOI PMC

Toews DP, Brelsford A. The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol. 2012;21(16):3907–30. 10.1111/j.1365-294X.2012.05664.x PubMed DOI

Gryseels S, Goüy de Bellocq J, Makundi R, Vanmechelen K, Broeckhove J, Mazoch V, et al. Genetic distinction between contiguous urban and rural multimammate mice in Tanzania despite gene flow. J Evol Biol. 2016. PubMed

Biek R, Real LA. The landscape genetics of infectious disease emergence and spread. Mol Ecol. 2010;19(17):3515–31. Epub 2010/07/14. PubMed Central PMCID: PMC3060346. 10.1111/j.1365-294X.2010.04679.x PubMed DOI PMC

Katakweba AAS, Mulungu LS, Eiseb SJ, Mahlaba TA, Makundi RH, Massawe AW, et al. Prevalence of haemoparasites, leptospires and coccobacilli with potential for human infection in the blood of rodents and shrews from selected localities in Tanzania, Namibia and Swaziland. Afr Zool. 2012;47(1):119–27.

Makundi RH, Massawe AW, Mulungu LS, Katakweba A. Species diversity and population dynamics of rodents in a farm-fallow field mosaic system in Central Tanzania. Afr J Ecol. 2010;48(2):313–20.

Makundi RH, Massawe AW, Borremans B, Laudisoit A, Katakweba A. We are connected: flea–host association networks in the plague outbreak focus in the Rift Valley, northern Tanzania. Wildlife Res. 2015;42(2):196–206.

Galan M, Van Hooft WF, Legrand D, Berthier K, Loiseau A, Granjon L, et al. A multiplex panel of microsatellite markers for widespread sub-Saharan rodents of the genus Mastomys. Mol Ecol Notes. 2004;4(3):321–3.

Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155(2):945–59. PubMed PMC

Hubisz MJ, Falush D, Stephens M, Pritchard JK. Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour. 2009;9(5):1322–32. 10.1111/j.1755-0998.2009.02591.x PubMed DOI PMC

Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I. Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour. 2015;15(5):1179–91. Epub 2015/02/17. PubMed Central PMCID: PMCPMC4534335. 10.1111/1755-0998.12387 PubMed DOI PMC

Stamatakis A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22(21):2688–90. 10.1093/bioinformatics/btl446 PubMed DOI

Food and Agriculture Organization of the United Nations (2015) Data from: FAO GEONETWORK. FAO. http://data.fao.org/ref/29400b68-42a5-4190-af8b-5f3e9d64d022.

McRae BH. Isolation by resistance. Evolution. 2006;60(8):1551–61. PubMed

Fields Development Team. fields: Tools for Spatial Data National Center for Atmospheric Research, Boulder, CO2006. Available from: http://www.cgd.ucar.edu/Software/Fields.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol. 2011;28(10):2731–9. 10.1093/molbev/msr121 PubMed DOI PMC

Goslee SC, Urban DL. The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw. 2007;22(7):1–19.

Baird SJE, Macholán M. What can the Mus musculus musculus / M. m. domesticus hybrid zone tell us about speciation? In: Macholán M, Baird SJE, Munclinger P, Piálek J, editors. Evolution of the House Mouse. 3 Cambridge: Cambridge University Press; 2012. p. 334.

Baird SJE, Barton NH. Analyse: Software for analysis of hybrid zones. 1995.

Li CC, Weeks DE, Chakravarti A. Similarity of DNA fingerprints due to chance and relatedness. Hum Hered. 1993;43(1):45–52. PubMed

Hardy OJ, Vekemans X. SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes. 2002;2(4):618–20.

Gryseels S, Baird SJE, Borremans B, Makundi R, Leirs H, Goüy de Bellocq J (2016) Data from: When viruses don’t go viral: the importance of host phylogeographic structure in the spatial spread of arenaviruses. Dryad Digital Repository. PubMed PMC

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space. Syst Biol. 2012;61(3):539–42. 10.1093/sysbio/sys029 PubMed DOI PMC

Guillot G, Rousset F. Dismantling the Mantel tests. Methods Ecol Evol. 2013;4(4):336–44.

de Menocal P, Ortiz J, Guilderson T, Adkins J, Sarnthein M, Baker L, et al. Abrupt onset and termination of the African Humid Period: rapid climate responses to gradual insolation forcing. Quat Sci Rev. 2000;19(1–5):347–61.

Borremans B, Leirs H, Gryseels S, Günther S, Makundi R, Goüy de Bellocq J. Presence of Mopeia Virus, an African arenavirus, related to biotope and individual rodent host characteristics; implications for virus transmission. Vector-Borne Zoonot Dis. 2011;11(8):1125–31. PubMed

Borremans B, Vossen R, Becker-Ziaja B, Gryseels S, Hughes N, Van Gestel M, et al. Shedding dynamics of Morogoro virus, an African arenavirus closely related to Lassa virus, in its natural reservoir host Mastomys natalensis. Sci Rep. 2015;5 http://www.nature.com/srep/2015/150529/srep10445/abs/srep10445.html—supplementary-information. PubMed PMC

Fichet-Calvet E, Becker-Ziaja B, Koivogui L, Gunther S. Lassa serology in natural populations of rodents and horizontal transmission. Vector-Borne Zoonot Dis. 2014;14(9):665–74. PubMed Central PMCID: PMC4170823. PubMed PMC

Wulff H, Lange J, Webb P. Interrelationships among arenaviruses measured by indirect immunofluorescence. Intervirology. 1978;9(6):344–50. PubMed

Meunier DY, McCormick JB, Georges AJ, Georges MC, Gonzalez JP. Comparison of Lassa, Mobala, and Ippy virus reactions by immunofluorescence test. The Lancet. 1985;325(8433):873–4. PubMed

Fisher-Hoch SP, Hutwagner L, Brown B, McCormick JB. Effective vaccine for lassa fever. J Virol. 2000;74(15):6777–83.PubMed Central PMCID: PMCPMC112194. PubMed PMC

Leirs H, Stenseth NC, Nichols JD, Hinds JE, Verhagen R, Verheyen W. Stochastic seasonality and nonlinear density-dependent factors regulate population size in an African rodent. Nature. 1997;389:176–80. 10.1038/38271 PubMed DOI

Luis AD, Hayman DTS, O'Shea TJ, Cryan PM, Gilbert AT, Pulliam JRC, et al. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proc Roy Soc B-Biol Sci. 2013;280(1756). Artn 20122753 PubMed PMC

Baird SJE, Ribas A, Macholán M, Albrecht T, Piálek J, Goüy de Bellocq J. Where Are the Wormy Mice? A Reexamination of Hybrid Parasitism in the European House Mouse Hybrid Zone. Evolution. 2012;66(9):2757–72. 10.1111/j.1558-5646.2012.01633.x PubMed DOI

Tayeh A, Tatard C, Kako-Ouraga S, Duplantier JM, Dobigny G. Rodent host cell/Lassa virus interactions: Evolution and expression of alpha-Dystroglycan, LARGE-1 and LARGE-2 genes, with special emphasis on the Mastomys genus. Infect Genet Evol. 2010;10(8):1262–70. 10.1016/j.meegid.2010.07.018 PubMed DOI

Kronmann KC, Nimo-Paintsil S, Guirguis F, Kronmann LC, Bonney K, Obiri-Danso K, et al. Two Novel Arenaviruses Detected in Pygmy Mice, Ghana. Emerg Infect Dis. 2013;19(11):1832 10.3201/eid1911.121491 PubMed DOI PMC

Brouat C, Tatard C, Ba K, Cosson JF, Dobigny G, Fichet-Calvet E, et al. Phylogeography of the Guinea multimammate mouse (Mastomys erythroleucus): a case study for Sahelian species in West Africa. J Biogeogr. 2009;36(12):2237–50.

Zobrazit více v PubMed

Dryad
10.5061/dryad.5n00k

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...