BACKGROUND: Parasite evolution is hypothesized to select for levels of parasite virulence that maximise transmission success. When host population densities fluctuate, low levels of virulence with limited impact on the host are expected, as this should increase the likelihood of surviving periods of low host density. We examined the effects of Morogoro arenavirus on the survival and recapture probability of multimammate mice (Mastomys natalensis) using a seven-year capture-mark-recapture time series. Mastomys natalensis is the natural host of Morogoro virus and is known for its strong seasonal density fluctuations. RESULTS: Antibody presence was negatively correlated with survival probability (effect size: 5-8% per month depending on season) but positively with recapture probability (effect size: 8%). CONCLUSIONS: The small negative correlation between host survival probability and antibody presence suggests that either the virus has a negative effect on host condition, or that hosts with lower survival probability are more likely to obtain Morogoro virus infection, for example due to particular behavioural or immunological traits. The latter hypothesis is supported by the positive correlation between antibody status and recapture probability which suggests that risky behaviour might increase the probability of becoming infected.

Bernhard Nocht Institute for Tropical Medicine Hamburg Germany

Department of Ecology and Evolutionary Biology University of Arizona Tucson USA

Department of Ecology and Evolutionary Biology University of California Los Angeles USA

Evolutionary Ecology Group University of Antwerp Antwerp Belgium

Institute of Vertebrate Biology Research Facility Studenec The Czech Academy of Sciences Brno Czech Republic

Interuniversity Institute for Biostatistics and statistical Bioinformatics Hasselt University Hasselt Belgium

Pest Management Center Sokoine University of Agriculture Morogoro Tanzania

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Anderson RM, May RM. Coevolution of hosts and parasites. Parasitology. 1982;85:411–426. doi: 10.1017/S0031182000055360. PubMed DOI

Ewald PW. Host-parasites relations, vectors, and the evolution of disease severity. Annu Rev Ecol Evol Syst. 1983:465–85.

Alizon S, Hurford A, Mideo N, Van Baalen M. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J Evol Biol. 2009;22:245–259. doi: 10.1111/j.1420-9101.2008.01658.x. PubMed DOI

Fraser C, Hollingsworth TD, Chapman R, de Wolf F, Hanage WP. Variation in HIV-1 set-point viral load: epidemiological analysis and an evolutionary hypothesis. Proc Natl Acad Sci USA. 2007;104:17441–174416. PubMed PMC

Doumayrou J, Avellan A, Froissart R, Michalakis Y. An experimental test of the tranmission-virulence trade-off hypothesis in a plant virus. Evolution. 2013;67:477–486. doi: 10.1111/j.1558-5646.2012.01780.x. PubMed DOI

Dwyer G, Levin S, Buttel L. A simulation model of the population dynamics and evolution of myxomatosis. Ecol Monogr. 2014;60:423–447. doi: 10.2307/1943014. DOI

Ebert D, Bull JJ. Challenging the trade-off model for the evolution of virulence: is virulence management feasible? Trends Microbiol. 2003;11:15–20. doi: 10.1016/S0966-842X(02)00003-3. PubMed DOI

Bull JJ, Lauring AS. Theory and empiricism in virulence evolution. PLoS Pathog. 2014;10:1–4. doi: 10.1371/journal.ppat.1004387. PubMed DOI PMC

King AA, Shrestha S, Harvill ET, Bjørnstad ON. Evolution of acute infections and the invasion-persistence trade-off. Am Nat. 2009;173:446–455. doi: 10.1086/597217. PubMed DOI PMC

Cressler CE, Mcleod DV, Rozins C, Van Den Hoogen J, Day T. The adaptive evolution of virulence: a review of theoretical predictions and empirical tests. Parasitology. 2016;143:915–930. doi: 10.1017/S003118201500092X. PubMed DOI PMC

Messinger SM, Ostling A. The consequences of spatial structure for the evolution of pathogen transmission rate and virulence. Am Nat. 2009;174:441–454. doi: 10.1086/605375. PubMed DOI

Boots B, Mealor M. Local interactions select for lower pathogen infectivity. Science. 2007;315:1284–1287. doi: 10.1126/science.1137126. PubMed DOI

Mariën J, Borremans B, Gryseels S, Soropogui B, De Bruyn L, Bongo GN, et al. No measurable adverse effects of Lassa, Morogoro and Gairo arenaviruses on their rodent reservoir host in natural conditions. Parasit Vectors. 2017;10:210. doi: 10.1186/s13071-017-2146-0. PubMed DOI PMC

Childs JE, CJ P. Ecology and epidemiology of arenaviruses and their hosts. In: Salvato M, editor. The Arenaviridae. New York: Plenum Press; 1993.

Gryseels S, Baird SJE, Borremans B, Makundi R, Leirs H, Goüy de Bellocq J. When viruses don’t go viral: the importance of host phylogeographic structure in the spatial spread of arenaviruses. PLoS Pathog. 2017;13:e1006073. PubMed PMC

McCormick JB. Lassa fever. Emergence. In: Dodet B, editor. Saluzzo JF. Heidelberg: Springer-Verlag; 2002.

World Health Organization. Lassa fever. Geneva: WHO; 2016. http://www.who.int/csr/disease/lassafever/en/. Accessed 13 June 2016.

Günther S, Lenz O. Lassa virus. Crit Rev Clin Lab Sci. 2004;41:339–390. doi: 10.1080/10408360490497456. PubMed DOI

Charrel RN, Coutard B, Baronti C, Canard B, Nougairede A, Frangeul A, et al. Arenaviruses and hantaviruses: from epidemiology and genomics to antivirals. Antivir Res. 2011;90:102–114. doi: 10.1016/j.antiviral.2011.02.009. PubMed DOI

Walker DH, Wulff H, Lange JV, Murphy FA. Comparative pathology of Lassa virus infection in monkeys, guinea-pigs, and Mastomys Natalensis. Bull World Health Organ. 1975;52:523–534. PubMed PMC

Webb P, Justines G, Johnson K. Infection of wild and laboratory animals with Machupo and Latino viruses. Bull World Health Organ. 1975;52:493–499. PubMed PMC

Oldstone MBA. Biology and pathogenesis of lymphocytic choriomeningitis virus infection. In: Clarke A, editor. Arenaviruses biology and immunoloy. Heidelberg: Springer-Verlag; 2002. 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. Nat Publ Gr. 2015;5:10445. 10.1038/srep%2010445. PubMed PMC

Weigand H, Hotchin J. Benson. The pathogenesis of lymphocytic choriomeningitis in mice: the effects of different inoculation routes and the footpad response. J Immunol. 1963;61:460–468. PubMed

Oldstone M, Dixon F. Susceptibility of different mouse strains to lymphocytic choriomeningitis virus. J Immunol. 1968;100:355–357. PubMed

Mims CA. Observations on mice infected congenitally or neonatally with lymphocytic choriomeningitis (LC31) Arch Ges Virusforsch. 1970;74:67–74. doi: 10.1007/BF01262584. PubMed DOI

Mariën J, Borremans B, Gryseels S, Vanden Broecke B, Becker-Ziaja B, Makundi R, et al. Arenavirus dynamics in experimentally and naturally infected rodents. EcoHealth. 2017;14:463. PubMed

Leirs H. Population ecology of Mastomys natalensis (Smith, 1834). Implications for rodent control in Africa. Agricultural edition 35. Brussels: Belgian Administration for Development Cooperation; 1994.

Sluydts V, Crespin L, Davis S, Lima M, Leirs H. Survival and maturation rates of the African rodent, Mastomys natalensis: density-dependence and rainfall. Integr Zool. 2007;2:220–32. PubMed

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

Günther S, Hoofd G, Charrel R, Röser C, Becker-Ziaja B, Lloyd G, et al. Mopeia virus-related arenavirus in natal multimammate mice, Morogoro, Tanzania. Emerg Infect Dis. 2009;15:2008–12. PubMed PMC

Goüy de Bellocq J, Borremans B, Katakweba A, Makundi R, SJE B, Becker-Ziaja B, et al. Sympatric occurrence of 3 arenaviruses, Tanzania. Emerg Infect Dis. 2010;16:692–695. doi: 10.3201/eid1604.091721. PubMed DOI PMC

Sluydts V, Davis S, Mercelis S, Leirs H. Comparison of multimammate mouse (Mastomys natalensis) demography in monoculture and mosaic agricultural habitat: implications for pest management. Crop Prot. 2009;28:647–654. doi: 10.1016/j.cropro.2009.03.018. DOI

Leirs H, Verheyen W, Michiels M, Verhagen R, Stuyck J. The relation between rainfall and the breeding season of Mastomys natalensis (Smith, 1834) in Morogoro, Tanzania. Ann Soc R Zool Belgique. 1990;119:59–64.

Borremans B, Reijniers J, Hughes NK, Godfrey SS, Gryseels S, Makundi RH, et al. Nonlinear scaling of foraging contacts with rodent population density. Oikos. 2016:1–9.

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

Borremans B, Sluydts V, Makundi RH, Leirs H. Evaluation of short-, mid- and long-term effects of toe clipping on a wild rodent. Wildl Res. 2015;42:143–148. doi: 10.1071/WR14109. DOI

Borremans B. Ammonium improves elution of fixed dried blood spots without affecting immunofluorescence assay quality. Tropical Med Int Health. 2014;19:413–416. doi: 10.1111/tmi.12259. PubMed DOI

Demby AH, Inapogui A, Kargbo K, Koninga J, Kourouma K, Kanu J, et al. Lassa fever in Guinea: II. Distribution and prevalence of Lassa virus infection in small mammals. Vector Borne Zoonotic Dis. 2001;1:283–99. doi: 10.1089/15303660160025912. PubMed DOI

R Core Team . R: a language and environment for statistical 688 computing. Vienna: R Foundation; 2016.

Laake JL, Johnson DS, Conn PB. Marked: an R package for maximum-likelihood and MCMC analysis of capture-recapture data. Methods Ecol Evol. 2013;4:885–890. doi: 10.1111/2041-210X.12065. DOI

White, G.C. and K. P. Burnham. 1999. Program MARK: survival estimation from populations of marked animals. Bird study 46 supplement, 120–138.

Johnson DS, Laake JL, Melin SR, DeLong RL. Multivariate state hidden Markov models for mark-recapture data. Stat Sci. 2016;31:233–244. doi: 10.1214/15-STS542. DOI

Pradel R, Wintrebert CMA, Gimenez O, Biometrics S, Mar N, Pradel R, et al. A proposal for a goodness-of-fit test to the Arnason-Schwarz multisite capture-recapture. Biometrics. 2003;59:43–53. doi: 10.1111/1541-0420.00006. PubMed DOI

Choquet R, Lebreton JD, Gimenez O, Reboulet AM, Pradel R. U-CARE: utilities for performing goodness of fit tests and manipulating CApture-REcapture data. Ecography. 2009;32:1071–1074. doi: 10.1111/j.1600-0587.2009.05968.x. DOI

Pradel R, Sanz-Aguilar A. Modeling trap-awareness and related phenomena in capture-recapture studies. PLoS One. 2012;7:3. doi: 10.1371/annotation/e240f425-0375-4c32-b0a7-85fa586d0f40. PubMed DOI PMC

Julliard R, Leirs H, Stenseth NC, Yoccoz NG, Prévot-Julliard AC, Verhagen R, et al. Survival-variation within and between functional categories of the African multimammate rat. J Anim Ecol. 1999;68:550–561. doi: 10.1046/j.1365-2656.1999.00304.x. DOI

Mi X, Miwa T, Hothorn T. mvtnorm: New numerical algorithm for multivariate normal probabilities. R J. 2009;1:37–39.

Gómez-Rubio V. ggplot2 - elegant graphics for data analysis (2nd edition) J Stat Softw. 2017;77:3–5. doi: 10.18637/jss.v077.b02. DOI

Verhagen R, Leirs H, Tkachenko E, van der Groen G. Ecological and epidemiological data on hantavirus in bank vole populations in Belgium. Arch Virol. 1986;91:193–205. doi: 10.1007/BF01314280. PubMed DOI

Bernshtein A, Apekina N, Mikhailova T, Myasnikov Y, Khlyap L, Korotkov Y, et al. Dynamics of Puumala hantavirus infection in naturally infected bank voles (Clethrinomys glareolus) Arch Virol. 1999;144:2415–2428. doi: 10.1007/s007050050654. PubMed DOI

Compton SR, Jacoby RO, Paturzo FX, Smith AL. Persistent Seoul virus infection in Lewis rats. Arch Virol. 2004;149:1325–1339. doi: 10.1007/s00705-004-0294-y. PubMed DOI PMC

Kallio ER, Voutilainen L, Vapalahti O, Vaheri A, Henttonen H, Mappes T, et al. Endemic hantavirus infection impairs the winter survival of its rodent host. Ecol Soc Am. 2011;88:1911–1916. PubMed

Tersago K, Crespin L, Verhagen R, Leirs H. Impact of Puumala virus infection on maturation and survival in bank voles: a capture-mark-recapture analysis. J Wildl Dis. 2012;48:148–156. doi: 10.7589/0090-3558-48.1.148. PubMed DOI

Luis AD, Douglass RJ, Hudson PJ, Mills JN, Bjørnstad ON. Sin Nombre hantavirus decreases survival of male deer mice. Oecologia. 2012;169:431–439. doi: 10.1007/s00442-011-2219-2. PubMed DOI

Bennett M, Crouch AJ, Begon M, Duffy B, Feore S, Gaskell RM, et al. Cowpox in British voles and mice. J Comp Pathol. 1997;116:35–44. doi: 10.1016/S0021-9975(97)80041-2. PubMed DOI

Chantrey J, Meyer H, Baxby D, Begon M, Bown KJ, Hazel SM, et al. Cowpox: reservoir hosts and geographic range. Epidemiol Infect. 1999;122:455–460. doi: 10.1017/S0950268899002423. PubMed DOI PMC

Telfer S, Bennett M, Bown K, Cavanagh R, Crespin L, Hazel S, et al. The effects of cowpox virus on survival in natural rodent populations : increases and decreases. J Anim Ecol. 2002;71:558–568. doi: 10.1046/j.1365-2656.2002.00623.x. DOI

Burthe S, Telfer S, Begon M, Bennett M, Smith A, Lambin X. Cowpox virus infection in natural field vole Microtus agrestis populations: significant negative impacts on survival. J Anim Ecol. 2008;77:110–119. doi: 10.1111/j.1365-2656.2007.01302.x. PubMed DOI PMC

Beldomenico PM, Telfer S, Lukomski L, Gebert S, Bennett M, Begon M. Host condition and individual risk of cowpox virus infection in natural animal populations: cause or effect? Epidemiol Infect. 2009;137:1295–1301. doi: 10.1017/S0950268808001866. PubMed DOI PMC

Barber I, Dingemanse NJ. Parasitism and the evolutionary ecology of animal personality. Philos Trans R Soc B Biol Sci. 2010;365:4077–4088. doi: 10.1098/rstb.2010.0182. PubMed DOI PMC

VanDen BB, Borremans B, Marien J, Makundi RH, Massawe AW, Leirs H, et al. Does exploratory behavior or activity in a wild mouse explain susceptibility to virus infection? Curr Zool. 2017;53:1–15. PubMed PMC

Boyer N, Réale D, Marmet J, Pisanu B, Chapuis JL. Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. J Anim Ecol. 2010;79:538–547. doi: 10.1111/j.1365-2656.2010.01659.x. PubMed DOI

Gold LH, Brot MD, Polis I, Schroeder R, Tishon A, de la Torre JC, et al. Behavioral effects of persistent lymphocytic choriomeningitis virus infection in mice. Behav Neural Biol. 1994;62:100–109. doi: 10.1016/S0163-1047(05)80031-7. PubMed DOI

De La Torre JC, Mallory M, Brot M, Gold L, Koob G, Oldstone MBA, et al. Viral persistence in neurons alters synaptic plasticity and cognitive functions without destruction of brain cells. Virology. 1996;220:508–515. doi: 10.1006/viro.1996.0340. PubMed DOI

Kunz S, Rojek JM, Roberts AJ, Mcgavern DB, Oldstone MBA, Carlos De La Torre J. Altered central nervous system gene expression caused by congenitally acquired persistent infection with lymphocytic choriomeningitis virus. J Virol. 2006;80:9082–9092. doi: 10.1128/JVI.00795-06. PubMed DOI PMC

Webster JP, Brunton CFA, Macdonald DW. Effect of Toxoplasma gondii upon neophobic behaviour in wild brown rats, Rattus norvegicus. Parasitology. 1994;109:37. PubMed

Sikes RS, Gannon WL. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal. 2007;88:809–823. doi: 10.1644/06-MAMM-F-185R1.1. PubMed DOI PMC