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Colonization history shaped the immunity of the western house mouse

  • Physiological ecology - Original research
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Abstract

The general development of immune response in the short and long term is a product of the antigenic environment in which a species resides. Colonization of a novel antigenic environment by a species would be expected to alter the immune system. Animals that successfully adapt their immune responses will successfully colonize new locations. However, founder events associated with colonization by limited numbers of individuals from a source population will constrain adaptability. How these contradicting forces shape immunity in widely distributed species is unknown. The western house mouse (Mus musculus domesticus) spread globally from the Indo-Pakistani cradle, often in association with human migration and settlement. In the present study, we tested the hypothesis that wild-derived outbred laboratory populations of house mice from their original range (Iran) and historically recent European invasive populations (from France and Germany) present differences in immune functional diversity corresponding to recent historical founder events in Europe and movement to novel antigenic environments. We found that (1) European mice had lower total white blood cell (WBC) counts but higher immunoglobulin E concentrations than their Iranian counterparts, and (2) there were no significant differences in the measured immunological parameters among European populations. The results indicate that founder events in European mice and selection pressure exerted by the composition of local parasitic helminth communities underlie the observed patterns.

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References

  • Allymehr M, Tavassoli M, Manoochehri MH, Ardavan D (2012) Ectoparasites and gastrointestinal helminths of house mice (Mus musculus) from poultry houses in Northwest Iran. Comp Parasitol 79:283–287

    Article  Google Scholar 

  • Aplin K, Ford F (2014) Murine rodents: late but highly successful invaders. In: Prins HHT, Gordan IJ (eds) Invasion biology and ecological theory: insights from a continent in transformation. Cambridge University Press, Cambridge, pp 196–240

    Chapter  Google Scholar 

  • Arim M, Abades SR, Neill PE, Lima M, Marquet PA (2006) Spread dynamics of invasive species. Proc Natl Acad Sci USA 103:374–378

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Auffray JC, Britton-Davidian J (2012) The house mouse and its relatives: systematics and taxonomy. In: Macholán M, Baird SJE, Munclinger P, Piálek J (eds) Evolution of the house mouse. Cambridge University Press, Cambridge, pp 1–34

    Chapter  Google Scholar 

  • Baines JF, Harr B (2007) Reduced X-linked diversity in derived populations of house mouse. Genetics 175:1911–1921

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Baired SJE, Ribas A, Macholán M, Albrecht T, Piálek J, de Bellocq JG (2012) Where are the wormy mice? A reexamination of hybrid parasitism in the European house mouse hybrid zone. Evolution 66:2757–2772

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc B 57:289–300

    Google Scholar 

  • Berry RJ (1986) Genetics of insular populations of mammals, with particular reference to differentiation and founder effects in British small mammals. Biol J Linn Soc 28:205–230

    Article  Google Scholar 

  • Bonhomme F, Searle JB (2012) House mouse phylogeography. In: Macholán M, Baird SJE, Munclinger P, Piálek J (eds) Evolution of the house mouse. Cambridge University Press, Cambridge, pp 278–296

    Chapter  Google Scholar 

  • Bonhomme F, Rivals E, Orth A, Grant GR, Jeffreys AJ, Bois PRJ (2007) Species-wide distribution of highly polymorphic minisatellite markers suggests past and present genetic exchanges among house mouse subspecies. Genome Biol 8:R80

    Article  PubMed Central  PubMed  Google Scholar 

  • Cesta MF (2006) Normal structure, function, and histology of the spleen. Toxicol Pathol 34:455–465

    Article  PubMed  Google Scholar 

  • Chai CK (1970) Genetic basis of leukocyte production in mice. J Hered 61:67–71

    CAS  PubMed  Google Scholar 

  • Chen J, Harrison DE (2002) Quantitative trait loci regulating relative lymphocyte proportions in mouse peripheral blood. Blood 99:561–566

    Article  CAS  PubMed  Google Scholar 

  • Corbin E, Vicente J, Martin-Hernando MP, Acevedo P, Pérez-Rodríguez L, Gortazar C (2008) Spleen mass as a measure of immune strength in mammals. Mammal Rev 38:108–115

    Article  Google Scholar 

  • Crowl TA, Crist TO, Parmenter RR, Belovsky G, Lugo AE (2008) The spread of invasive species and infectious disease as drivers of ecosystem change. Front Ecol Environ 6:238–246

    Article  Google Scholar 

  • Cucchi T, Vigne JD, Auffray JC (2005) First occurrence of the house mouse (Mus musculus domesticus Schwarz & Schwarz, 1943) in the Western Mediterranean: a zooarchaeological revision of subfossil occurrences. Biol J Linn Soc 84:429–445

    Article  Google Scholar 

  • Cucchi T, Auffray JC, Vigne JD (2012) On the origin of house mouse synanthropy and dispersal in the near East and Europe: zooarchaeological review and perspectives. In: Macholán M, Baird SJE, Munclinger P, Piálek J (eds) Evolution of the house mouse. Cambridge University Press, Cambridge, pp 65–93

    Chapter  Google Scholar 

  • Feliu C, López M, Gómez MS, Torres J, Sánchez S, Miquel J, Abreu-Acosta N, Segovia JM, Martín-Alonso A, Montoliu I, Villa M, Fernández-Álvarez Á, Bakhoum AJS, Valladares B, Orós J, Foronda P (2012) Parasite fauna of rodents (Murinae) from El Hierro (Canary Islands, Spain): a multidisciplinary approach. Acta Parasitol 57:171–178

    Article  PubMed  Google Scholar 

  • Goüy de Bellocq J, Porcherie A, Moulia C, Morand S (2007) Immunocompetence does not correlate with resistance to helminth parasites in house mouse subspecies and their hybrids. Parasitol Res 100:321–328

    Article  PubMed  Google Scholar 

  • Gray MM, Wegmann D, Haasl RJ, White MA, Gabriel SI, Searle JB, Cuthert RJ, Ryan PG, Payseur BA (2014) Demographic history of a recent invasion of house mice on the isolated Island of Gough. Mol Ecol 23:1923–1939

    Article  PubMed Central  PubMed  Google Scholar 

  • Hájek J, Šidák Z, Sen PK (1999) Theory of rank tests, 2nd edn. Academic, San Diego

  • Hufbauer RA, Torchin ME (2007) Integrating ecological and evolutionary theory of biological invasions. In: Nentwig W (ed) Biological invasions. Springer, Berlin, pp 79–96

  • Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18

    Article  Google Scholar 

  • Keller RP, Geist J, Jeschke JM, Kühn I (2011) Invasive species in Europe: ecology, status, and policy. Env Sci Eur 23:23

    Article  Google Scholar 

  • Kia EB, Homayouni MM, Farahnak A, Mohebali M, Shojai S (2001) Study of endoparasites of rodents and their zoonotic importance in Ahvaz, South West Iran. Iran J Public Health 30:49–52

    Google Scholar 

  • Lee KA, Klasing KC (2004) A role for immunology in invasion biology. Trends Ecol Evol 19:523–529

    Article  PubMed  Google Scholar 

  • Lee KA, Martin LB, Wikelski MC (2005) Responding to inflammatory challenges is less costly for a successful avian invader, the house sparrow (Passer domesticus), than its less-invasive congener. Oecologia 145:244–251

    Article  PubMed  Google Scholar 

  • Llewellyn D, Thompson MB, Brown GP, Phillips BL, Shine R (2012) Reduced investment in immune function in invasion-front populations of the cane toad (Rhinella marina) in Australia. Biol Invasions 14:999–1008

    Article  Google Scholar 

  • Manjerovic MB, Waterman JM (2012) Immunological sex differences in socially promiscuous African ground squirrels. PLoS One 7:e38524

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martin LB, Liebl AL, Kilvitis HJ (2015) Covariation in stress and immune gene expression in a range expanding bird. Gen Comp Endocrinol 211:14–19

    Article  CAS  PubMed  Google Scholar 

  • Mebius RE, Kraal G (2005) Structure and function of the spleen. Nat Rev Immunol 5:606–616

    Article  CAS  PubMed  Google Scholar 

  • Milazzo C, De Bellocq JG, Cagnin M, Casanova JC, Di Bella C, Feliu C, Fons R, Morand S, Santalla F (2003) Helminths and ectoparasites of Rattus rattus and Mus musculus from Sicily, Italy. Comp Parasitol 70:99–104

    Article  Google Scholar 

  • Milazzo C, Cagnin M, Di Bella C, Geraci F, Ribas A (2010) Helminth fauna of commensal rodents, Mus musculus (Linnaeus, 1758) and Rattus rattus (Linnaeus, 1758) (Rodentia, Muridae) in Sicily (Italy). Rev Ibero-Latinoam Parasitol 69:194–198

    Google Scholar 

  • Møller AP, Sorci G, Erritzøe J (1998) Sexual dimorphism in immune defense. Am Nat 152:605–619

    Article  PubMed  Google Scholar 

  • Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci USA 98:5446–5451

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Morand S, Bordes F, Chen H-W, Claude J, Cosson J-F, Galan M, Czirják GÁ, Greenwood AD, Latinne A, Michaux J, Ribas A (2015) Global parasite and Rattus rodent invasions: the consequences for rodent-borne diseases. Integr Zool (in press). doi:10.1111/1749-4877.12143

  • Murphy K (2012) Janeway’s immunobiology, 8th edn. Garland Science, London

    Google Scholar 

  • Pakdel N, Naem S, Rezaei F, Chalehchaleh AA (2013) A survey on helminthic infection in mice (Mus musculus) and rats (Rattus norvegicus and Rattus rattus) in Kermanshah. Iran. Vet Res Forum 4:105–109

    PubMed  Google Scholar 

  • Phillips BL, Brown GP, Shine R (2010) Life-history evolution in range-shifting populations. Ecology 91:1617–1627

    Article  PubMed  Google Scholar 

  • Ponlet N, Chaisiri K, Claude J, Morand S (2011) Incorporating parasite systematics in comparative analyses of variation in spleen mass and testes sizes of rodents. Parasitology 138:1804–1814

    Article  PubMed  Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org. Accessed 31 Oct 2014

  • Rajabi-Maham H, Orth A, Bonhomme F (2008) Phylogeography and postglacial expansion of Mus musculus domesticus inferred from mitochondrial DNA coalescent, from Iran to Europe. Mol Ecol 17:627–641

    Article  CAS  PubMed  Google Scholar 

  • Rapp KG (1972) HAN-rotation, a new system for rigorous outbreeding. Z Versuchstierkd 14:133–142

    CAS  PubMed  Google Scholar 

  • Schulte-Hostedde AI, Elsasser SC (2011) Spleen mass, body condition, and parasite load in male American mink (Neovison vison). J Mammal 92:221–226

    Article  Google Scholar 

  • Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, García-Berthou E, Pascal M, Pyšek P, Sousa R, Tabacchi E, Vilà M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66

    Article  PubMed  Google Scholar 

  • Suzuki H, Nunome M, Kinoshita G, Aplin KP, Vogel P, Kryukov AP, Jin M-L, Han S-H, Maryanto I, Tsuchiya K, Ikeda H, Shiroishi T, Yonekawa H, Moriwaki K (2013) Evolutionary and dispersal history of Eurasian house mice Mus musculus clarified by more extensive geographic sampling of mitochondrial DNA. Heredity 111:375–390

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Swamy PM (2009) Laboratory manual on biotechnology. Rastogi, Meerut

  • Swan MP, Hickman DL (2014) Evaluation of the neutrophil–lymphocyte ratio as a measure of distress in rats. Lab Anim (NY) 43:276–282

  • Tian JD, Courtiol A, Schneeberger K, Greenwood AD, Czirják GÁ (2015) Circulating white blood cell counts in captive and wild rodent are influenced by body mass rather than testes mass, a correlate of mating promiscuity. Funct Ecol 29:823–829

    Article  Google Scholar 

  • Weir JA, Schlager G (1962) Selection for leucocyte count in the house mouse and some physiological effects. Genetics 47:1199–1217

    PubMed Central  CAS  PubMed  Google Scholar 

  • White TA, Perkins SE (2012) The ecoimmunology of invasive species. Funct Ecol 26:1313–1323

    Article  Google Scholar 

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Acknowledgments

We thank Diethard Tautz for providing access to samples from the house mice. We are grateful to Natascha Hasenkamp, Heike Harre, Christine Pfeifle, Heinke Buhtz, Cornelia Burghardt, and the mouse housing team from the Max Planck Institute for Evolutionary Biology, Plön as well as Katja Pohle from the Leibniz Institute for Zoo and Wildlife Research, Berlin for their technical and logistical assistance. Further thanks are due to Anca Dorhoi from the Max Planck Institute for Infection Biology for commenting on the immunological interpretation. J.D. Tian is supported by a Ph.D. scholarship from the China Scholarship Council (no. 2011704029). This research was supported by funds from the Leibniz Institute for Zoo and Wildlife Research.

Author contribution statement

ADG and GÁC conceived and designed the experiments. JT performed the experiments. JT and HH analyzed the data. JT, ADG, HH, and GÁC wrote the manuscript.

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Authors and Affiliations

  1. Department of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315, Berlin, Germany

    Jundong Tian, Alex D. Greenwood & Gábor Á. Czirják

  2. Department of Veterinary Medicine, Freie Universität Berlin, 14163, Berlin, Germany

    Jundong Tian

  3. Department of Evolutionary Ecology, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315, Berlin, Germany

    Heribert Hofer

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  1. Jundong Tian
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Correspondence to Gábor Á. Czirják.

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Communicated by Pawel Koteja.

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442_2015_3397_MOESM1_ESM.doc

Fig. S1. Interactive effects of house mouse body mass and three sampling sites on the immunological variables measured. There are no obvious interactions of total WBC (a), IgE (b), IgG (c), and IgM (d) with body mass for French, German, and Iranian wild-derived outbred laboratory house mice. (DOC 106 kb)

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Tian, J., Hofer, H., Greenwood, A.D. et al. Colonization history shaped the immunity of the western house mouse. Oecologia 179, 679–686 (2015). https://doi.org/10.1007/s00442-015-3397-0

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