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Wild cyclic voles maintain high neutral and MHC diversity without strong evidence for parasite-mediated selection

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Abstract

The major histocompatibility complex (MHC) is an important component of vertebrate immune defense involved with self/nonself recognition and disease susceptibility. The high variability of genes of the MHC is thought to arise from both parasite-mediated and sexual selection. An outstanding question involves the degree to which balancing selection can oppose genetic drift to maintain high MHC diversity in the face of population bottlenecks. To address this question we examined genetic diversity and population structure at neutral (microsatellite) and MHC genes in montane voles [Microtus montanus (Peale, 1848)] subject to high amplitude population fluctuations, and compared these to measures of infection by common gastrointestinal parasites. We found high neutral and MHC allelic variability, indicating low impacts of genetic drift despite large fluctuations in population size. Greater MHC diversity did not predict lower parasite richness or infection by the two most common endoparasites (cestodes and coccidian protozoa), as might be expected if genotypic composition confers resistance to infection. One specific MHC allele predicted lower cestode intensity, but we found no other associations between MHC and infection measures. Neutral heterozygosity was positively associated with total parasite richness, possibly owing to greater parasite tolerance among heterozygous relative to more inbred hosts. Overall, these results suggest that factors beyond the parasites examined here, such as high inter-patch migration, mate choice, gene conversion or other infectious agents, are likely maintaining the high levels of MHC diversity observed in wild montane voles.

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References

  • Acevedo-Whitehouse K, Gulland F, Greig D, Amos W (2003) Inbreeding: disease susceptibility in California sea lions. Nature 422:35

    CAS  PubMed  Google Scholar 

  • Acevedo-Whitehouse K, Vicente J, Gortazar C, Hofle U, Fernandez-De-Mera IG, Amos W (2005) Genetic resistance to bovine tuberculosis in the Iberian wild boar. Mol Ecol 14:3209–3217

    CAS  PubMed  Google Scholar 

  • Aguilar A, Roemer G, Debenham S, Binns M, Garcelon D, Wayne RK (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci USA 101:3490–3494

    CAS  PubMed Central  PubMed  Google Scholar 

  • Apanius V, Penn D, Slev PR, Ruff LR, Potts WK (1997) The nature of selection on the major histocompatibility complex. Crit Rev Immunol 17:179–224

    CAS  PubMed  Google Scholar 

  • Axtner J, Sommer S (2012) The functional importance of sequence versus expression variability of MHC alleles in parasite resistance. Genetica 140:407–420

    Google Scholar 

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

    PubMed  Google Scholar 

  • Bakke TA, Wiger R (1975) Endoparasites of selected small rodents and their predators with special reference to pathology. Ecol Bull 19:201–207

    Google Scholar 

  • Barton N, Slatkin M (1986) A quasi-equilibrium theory of the distribution of rare alleles in a subdivided population. Heredity 56:409–415

    PubMed  Google Scholar 

  • Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16:363–377

    CAS  PubMed  Google Scholar 

  • Berthier K, Charbonnel N, Galan M, Chaval Y, Cosson JF (2006) Migration and recovery of the genetic diversity during the increasing density phase in cyclic vole populations. Mol Ecol 15:2665–2676

    CAS  PubMed  Google Scholar 

  • Bryja J, Charbonnel N, Berthier K, Galan M, Cosson JF (2007) Density-related changes in selection pattern for major histocompatibility complex genes in fluctuating populations of voles. Mol Ecol 16:5084–5097

    CAS  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Calcagno V, de Mazancourt C (2010) glmulti: an R package for easy automated model selection with (generalized) linear models. J Stat Softw 34:1–29

    Google Scholar 

  • Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred soay sheep in a free-living, island population. Evolution 53:1259–1267

    Google Scholar 

  • Coulson T, Pemberton J, Albon S, Beaumont M, Marshall T, Slate J, Guinness F, Clutton-Brock T (1998) Microsatellites reveal heterosis in red deer. In: Proceedings of the Royal Society of London. Series B: Biological Sciences, vol 265, pp 489–495

  • Crawford NG (2009) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10:556–557

    PubMed  Google Scholar 

  • Doherty PC, Zinkernagel RM (1975) Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256:50–52

    CAS  PubMed  Google Scholar 

  • Doytchinova IA, Flower DR (2005) In silico identification of supertypes for Class II MHCs. J Immunol 174:7085–7095

    CAS  PubMed  Google Scholar 

  • Edwards SV, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13:305–311

    CAS  PubMed  Google Scholar 

  • Eizaguirre C, Lenz TL, Kalbe M, Milinski M (2012) Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations. Nat Commun 3:621

    PubMed Central  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  PubMed Central  Google Scholar 

  • Faircloth BC, Glenn TC (2011) Large sets of edit-metric sequence identification tags to facilitate large-scale multiplexing of reads from massively parallel sequencing. Nat. Proc. http://hdl.handle.net/10101/npre.2011.5672.1

  • Ferrari N, Cattadori IM, Nespereira J, Rizzoli A, Hudson PJ (2004) The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecol Lett 7:88–94

    Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge, p 617

    Google Scholar 

  • Fraser BA, Ramnarine IW, Neff BD (2010) Temporal variation at the MHC class IIB in wild populations of the guppy (Poecilia reticulata). Evolution 64:2086–2096

    PubMed  Google Scholar 

  • Froeschke G, Sommer S (2005) MHC class II DRB variability and parasite load in the striped mouse (Rhabdomys pumilio) in the southern Kalahari. Mol Biol Evol 22:1254–1259

    CAS  PubMed  Google Scholar 

  • Froeschke G, Sommer S (2012) Insights into the complex associations between MHC Class II DRB polymorphism and multiple gastrointestinal parasite infestations in the striped mouse. PLoS ONE 7:e31820

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fuller CA, Blaustein AR (1996) Effects of the parasite Eimeria arizonensis on survival of deer mice (Peromyscus maniculatus). Ecology 77:2196–2202

    Google Scholar 

  • Galan M, Guivier E, Caraux G, Charbonnel N, Cosson JF (2010) A 454 multiplex sequencing method for rapid and reliable genotyping of highly polymorphic genes in large-scale studies. BMC Genom 11:296

    Google Scholar 

  • Garrigan D, Hedrick PW (2003) Perspective: detecting adaptive molecular polymorphism: Lessons from the MHC. Evolution 57:1707–1722

    CAS  PubMed  Google Scholar 

  • Gauffre B, Galan M, Bretagnolle V, Cosson J (2007) Polymorphic microsatellite loci and PCR multiplexing in the common vole, Microtus arvalis. Mol Ecol Notes 7:830–832

    CAS  Google Scholar 

  • Goudet J (2001) FSTAT, version 2.9.3, a program to estimate and test gene diversities and fixation indices. Lausanne University, Lausanne

  • Grueber C, Nakagawa S, Laws R, Jamieson I (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711

    CAS  PubMed  Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Google Scholar 

  • Hakkarainen H, Huhta E, Koskela E, Mappes T, Soveri T, Suorsa P (2006) Eimeria-parasites are associated with a lowered mother’s and offspring’s body condition in island and mainland populations of the bank vole. Parasitology 134:23–31

    PubMed  Google Scholar 

  • Hass CC (1989) Bighorn lamb mortality: predation, inbreeding, and population effects. Can J Zool 67:699–705

    Google Scholar 

  • Havlicek J, Roberts SC (2009) MHC-correlated mate choice in humans: a review. Psychoneuroendocrinology 34:497–512

    CAS  PubMed  Google Scholar 

  • Hedrick P (2004) Evolutionary genomics: Foxy MHC selection story. Heredity 93:237–238

    CAS  PubMed  Google Scholar 

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

    CAS  PubMed  Google Scholar 

  • Hess G, Randolph S, Arneberg P, Chemini C, Furlanello C, Harwood J, Roberts M, Swinton J (2002) Spatial aspects of disease dynamics. In: Hudson P, Rizzoli A, Grenfell B, Heesterbeek H, Dobson A (eds) The ecology of wildlife diseases. Oxford University Press, Oxford, pp 102–118

    Google Scholar 

  • Hill AVS, Allsopp CEM, Kwiatkowski D, Anstey NM, Twumasi P, Rowe PA, Bennett S, Brewster D, McMichael AJ, Greenwood BM (1991) Common West African HLA antigens are associated with protection from severe malaria. Nature 352:595–600

    CAS  PubMed  Google Scholar 

  • Hughes AL, Yeager M (1998) Natural selection at major histocompatibility complex loci of vertebrates. Annu Rev Genet 32:415

    CAS  PubMed  Google Scholar 

  • Jamieson IG, Tracy LN, Fletcher D, Armstrong DP (2007) Moderate inbreeding depression in a reintroduced population of North Island robins. Anim Conserv 10:95–102

    Google Scholar 

  • Johnson WE, Onorato DP, Roelke ME, Land ED, Cunningham M, Belden RC, McBride R, Jansen D, Lotz M, Shindle D, Howard J, Wildt DE, Penfold LM, Hostetler JA, Oli MK, O’Brien SJ (2010) Genetic restoration of the florida panther. Science 329:1641–1645

    CAS  PubMed  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Google Scholar 

  • Keller LF, Arcese P, Smith JNM, Hochachka WM, Stearns SC (1994) Selection against inbred song sparrows during a natural population bottleneck. Nature 372:356–357

    CAS  PubMed  Google Scholar 

  • Keymer AE, Hiorns RW (1986) Faecal egg counts and nematode fecundity: heligmosomoides polygyrus and laboratory mice. Parasitology 93:189–203

    PubMed  Google Scholar 

  • Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New York

    Google Scholar 

  • Kloch A, Baran K, Buczek M, Konarzewski M, Radwan J (2013) MHC influences infection with parasites and winter survival in the root vole Microtus oeconomus. Evol Ecol 27:635–653

    Google Scholar 

  • Knapp LA (2005) The ABCs of MHC. Evol Anthropol Issues News Rev 14:28–37

    Google Scholar 

  • Korpimäki E, Norrdahl K, Klemola T, Pettersen T, Stenseth NC (2002) Dynamic effects of predators on cyclic voles: field experimentation and model extrapolation. In: Proceedings of the Royal Society of London. Series B: Biological Sciences, vol 269, pp 991–997

  • Krebs CJ (1996) Population cycles revisited. J Mammal 77:8–24

    Google Scholar 

  • Krebs CJ (2013) Population fluctuations in rodents. University of Chicago Press, Chicago

    Google Scholar 

  • Lello J, Boag B, Hudson PJ (2005) The effect of single and concomitant pathogen infections on condition and fecundity of the wild rabbit (Oryctolagus cuniculus). Int J Parasitol 35:1509–1515

    CAS  PubMed  Google Scholar 

  • Levine ND, Ivens V (1965) The coccidian parasties (Protozoa, Sporozoa) of rodents. University of Illinois Press, Urbana

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  PubMed  Google Scholar 

  • Lillehoj HS, Ruff MD, Bacon LD, Lamont SJ, Jeffers TK (1989) Genetic control of immunity to Eimeria tenella. Interaction of MHC genes and non-MHC linked genes influences levels of disease susceptibility in chickens. Vet Immunol Immunopathol 20:135–148

    CAS  PubMed  Google Scholar 

  • Milinski M (2006) The major histocompatibility complex, sexual selection, and mate choice. Annu Rev Ecol Evol Syst 37:159–186

    Google Scholar 

  • Miller HC, Lambert DM (2004) Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Mol Ecol 13:3709–3721

    CAS  PubMed  Google Scholar 

  • Miller HC, Allendorf F, Daugherty CH (2010) Genetic diversity and differentiation at MHC genes in island populations of tuatara (Sphenodon spp.). Mol Ecol 19:3894–3908

    PubMed  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nei M, Chesser RK (1983) Estimation of fixation indices and gene diversities. Ann Hum Genet 47:253–259

    CAS  PubMed  Google Scholar 

  • Oliver MK, Piertney SB (2012) Selection maintains MHC diversity through a natural population bottleneck. Mol Biol Evol 29:1713–1720

    CAS  PubMed  Google Scholar 

  • Oliver MK, Lambin X, Cornulier T, Piertney SB (2009a) Spatio-temporal variation in the strength and mode of selection acting on major histocompatibility complex diversity in water vole (Arvicola terrestris) metapopulations. Mol Ecol 18:80–92

    CAS  PubMed  Google Scholar 

  • Oliver MK, Telfer S, Piertney SB (2009b) Major histocompatibility complex (MHC) heterozygote superiority to natural multi-parasite infections in the water vole (Arvicola terrestris). Proc R Soc B Biol Sci 276:1119–1128

    CAS  Google Scholar 

  • Paul WE, Zhu J (2010) How are TH2-type immune responses initiated and amplified? Nat Rev Immunol 10:225–235

    Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Google Scholar 

  • Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility complex genes. Am Nat 153:145–164

    Google Scholar 

  • Penn DJ, Damjanovich K, Potts WK (2002) MHC heterozygosity confers a selective advantage against multiple-strain infections. Proc Natl Acad Sci 99:11260–11264

    CAS  PubMed Central  PubMed  Google Scholar 

  • Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21

    CAS  PubMed  Google Scholar 

  • Pinter AJ (1986) Population-dynamics and litter size of the montane vole, Microtus montanus. Can J Zool Revue Canadienne De Zoologie 64:1487–1490

    Google Scholar 

  • Radwan J, Biedrzycka A, Babik W (2010) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 143:537–544

    Google Scholar 

  • Raymond M, Rousset F (1995a) An exact test for population differentiation. Evolution 49:1280–1283

    Google Scholar 

  • Raymond M, Rousset F (1995b) Genepop (version-1.2)—population-genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103

    CAS  PubMed  Google Scholar 

  • Rijks J, Hoffman J, Kuiken T, Osterhaus A, Amos W (2008) Heterozygosity and lungworm burden in harbour seals (Phoca vitulina). Heredity 100:587–593

    CAS  PubMed  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    PubMed  Google Scholar 

  • Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494

    CAS  Google Scholar 

  • Sandberg M, Eriksson L, Jonsson J, Sjöström M, Wold S (1998) New chemical descriptors relevant for the design of biologically active peptides. A multivariate characterization of 87 amino acids. J Med Chem 41:2481–2491

    CAS  PubMed  Google Scholar 

  • Schad J, Sommer S, Ganzhorn JU (2004) MHC variability of a small lemur in the littoral forest fragments of southeastern Madagascar. Conserv Genet 5:299–309

    CAS  Google Scholar 

  • Schad J, Dechmann DKN, Voigt CC, Sommer S (2012) Evidence for the ‘good genes’ model: association of MHC Class II DRB alleles with ectoparasitism and reproductive state in the neotropical lesser bulldog bat, Noctilio albiventris. PLoS ONE 7:e37101

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schito ML, Barta JR, Chobotar B (1996) Comparison of four murine Eimeria species in immunocompetent and immunodeficient mice. J Parasitol 82:255–262

    CAS  PubMed  Google Scholar 

  • Schwensow N, Fietz J, Dausmann KH, Sommer S (2007) Neutral versus adaptive genetic variation in parasite resistance: importance of major histocompatibility complex supertypes in a free-ranging primate. Heredity 99:265–277

    CAS  PubMed  Google Scholar 

  • Scott ME (1988) The impact of infection and disease on animal populations: implications for conservation biology. Conserv Biol 2:40–56

    Google Scholar 

  • Scott ME, Lewis JW (1987) Population dynamics of helminth parasites in wild and laboratory rodents. Mammal Rev 17:95–103

    Google Scholar 

  • Sera WE, Early CN (2003) Microtus montanus. Mamm Species 716:1–10

    Google Scholar 

  • Sikes RS, Gannon WL (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92:235–253

    Google Scholar 

  • Smith A, Telfer S, Burthe S, Bennett M, Begon M (2005) Trypanosomes, fleas and field voles: ecological dynamics of a host-vector-parasite interaction. Parasitology 131:355–365

    CAS  PubMed  Google Scholar 

  • Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:1742–1760

    Google Scholar 

  • Spielman D, Brook BW, Briscoe DA, Frankham R (2004a) Does inbreeding and loss of genetic diversity decrease disease resistance? Conserv Genet 5:439–448

    Google Scholar 

  • Spielman D, Brook BW, Frankham R (2004b) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101:15261–15264

    CAS  PubMed Central  PubMed  Google Scholar 

  • Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R S B Biol Sci 277:979–988

    CAS  Google Scholar 

  • Spurgin LG, van Oosterhout C, Illera JC, Bridgett S, Gharbi K, Emerson BC, Richardson DS (2011) Gene conversion rapidly generates major histocompatibility complex diversity in recently founded bird populations. Mol Ecol 20:5213–5225

    CAS  PubMed  Google Scholar 

  • Stenseth NC (1999) Population cycles in voles and lemmings: density dependence and phase dependence in a stochastic world. Oikos 87:427–461

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Storey JD (2002) A direct approach to false discovery rates. J R Stat Soc Ser B (Stat Methodol) 64:479–498

    Google Scholar 

  • Sutton JT, Nakagawa S, Robertson BC, Jamieson IG (2011) Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes. Mol Ecol 20:4408–4420

    PubMed  Google Scholar 

  • Symonds MR, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21

    Google Scholar 

  • Takahata N, Nei M (1990) Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124:967–978

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    CAS  PubMed Central  PubMed  Google Scholar 

  • Team RDC (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing Vienna, Austria

    Google Scholar 

  • Thompson JN (1998) Rapid evolution as an ecological process. Trends Ecol Evol 13:329–332

    CAS  PubMed  Google Scholar 

  • Tollenaere C, Bryja J, Galan M, Cadet P, Deter J, Chaval Y, Berthier K, Ribas Salvador A, Voutilainen L, Laakkonen J, Henttonen H, Cosson JF, Charbonnel N (2008) Multiple parasites mediate balancing selection at two MHC class II genes in the fossorial water vole: insights from multivariate analyses and population genetics. J Evol Biol 21:1307–1320

    CAS  PubMed  Google Scholar 

  • Townsend SM, Jamieson IG (2013) Inbreeding influences within-brood heterozygosity-fitness correlations (HFCS) in an isolated passerine population. Evolution 67:2299–2308

    PubMed  Google Scholar 

  • Turner WC, Versfeld WD, Kilian JW, Getz WM (2012) Synergistic effects of seasonal rainfall, parasites and demography on fluctuations in springbok body condition. J Anim Ecol 81:58–69

    PubMed Central  PubMed  Google Scholar 

  • Van de Zande L, Van Apeldoorn R, Blijdenstein A, De Jong D, Van Delden W, Bijlsma R (2000) Microsatellite analysis of population structure and genetic differentiation within and between populations of the root vole, Microtus oeconomus in the Netherlands. Mol Ecol 9:1651–1656

    PubMed  Google Scholar 

  • Van oosterhout C, Van oosterhout WF, Wills DPM, Shipley P (2004) Micro- checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    CAS  Google Scholar 

  • van Oosterhout C, Joyce DA, Cummings SM, Blais J, Barson NJ, Ramnarine IW, Mohammed RS, Persad N, Cable J (2006) Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata). Evolution 60:2562–2574

    PubMed  Google Scholar 

  • Vorisek P, Votypka J, Zvara K, Svobodova M (1998) Heteroxenous coccidia increase the predation risk of parasitized rodents. Parasitology 117:521–524

    PubMed  Google Scholar 

  • Walser B, Heckel G (2008) Microsatellite markers for the common vole (Microtus arvalis) and their cross-species utility. Conserv Genet 9:479–481

    CAS  Google Scholar 

  • Watkins RA, Moshier SE, O’Dell WD, Pinter AJ (1991) Splenomegaly and reticulocytosis caused by Babesia microti infections in natural populations of the montane vole, Microtus montanus. J Eukaryot Microbiol 38:573–576

    Google Scholar 

  • Wegner KM, Kalbe M, Kurtz J, Reusch TBH, Milinski M (2003) Parasite selection for immunogenetic optimality. Science 301:1343

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Google Scholar 

  • Westerdahl H, Waldenstrom J, Hansson B, Hasselquist D, von Schantz T, Bensch S (2005) Associations between malaria and MHC genes in a migratory songbird. Proc R Soc B Biol Sci 272:1511–1518

    CAS  Google Scholar 

  • Westerdahl H, Stjernman M, Råberg L, Lannefors M, Nilsson J-Å (2013) MHC-I affects infection intensity but not infection status with a frequent avian malaria parasite in blue tits. PLoS ONE 8:e72647

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wiger R (1977) Some pathological effects of endoparasites on rodents with special reference to the population ecology of microtines. Oikos 29:598–606

    Google Scholar 

  • Winternitz JC, Wares JP (2013) Duplication and population dynamics shape historic patterns of selection and genetic variation at the major histocompatibility complex in rodents. Ecol Evol 3:1552–1568

    PubMed Central  PubMed  Google Scholar 

  • Winternitz J, Yabsley M, Altizer S (2012) Parasite infection and host dynamics in a naturally fluctuating rodent population. Can J Zool 90:1149–1160

    Google Scholar 

  • Winternitz JC, Minchey SG, Garamszegi LZ, Huang S, Stephens PR, Altizer S (2013) Sexual selection explains more functional variation in the mammalian major histocompatibility complex than parasitism. Proc R Soc B Biol Sci 280

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Acknowledgments

We thank the Rocky Mountain Biological Laboratory for field site coordination and J. Brancale, L. Bryant, M. Eisel, P. Howell, J. Lieb, and J. Parmer for trapping assistance. T. Glenn provided advice and resources for molecular genetic work, and J. Carroll, J. Moore, and the Altizer and Ezenwa lab groups at UGA, and two anonymous reviewers provided useful discussion and comments on previous manuscript drafts. We thank the Odum School of Ecology, National Geographic Society, Animal Behavior Society, Association for Women in Science, Philosophical Society, and the Rocky Mountain Biological Laboratory for funding of field and lab work. JCW was supported by a Graduate School Assistantship from the University of Georgia and a T-32 Training Grant from the National Institutes of Health. SA was supported by funding from the National Science Foundation (DEB-0643831 and DEB-1020966). JPW was supported by funding from the National Science Foundation (NSF-OCE-1029526).

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  1. J. C. Winternitz

    Present address: Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, v.v.i., Květná 8, 603 65, Brno, Czech Republic

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  1. Odum School of Ecology, University of Georgia, Athens, GA, 30602, USA

    J. C. Winternitz & S. Altizer

  2. Department of Genetics, University of Georgia, Athens, GA, 30602, USA

    J. P. Wares

  3. College of Veterinary Medicine, University of Georgia, Athens, GA, 30602, USA

    M. J. Yabsley

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Winternitz, J.C., Wares, J.P., Yabsley, M.J. et al. Wild cyclic voles maintain high neutral and MHC diversity without strong evidence for parasite-mediated selection. Evol Ecol 28, 957–975 (2014). https://doi.org/10.1007/s10682-014-9709-8

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