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Sex and the Red Queen

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Lost Sex

Abstract

Negative frequency-dependent selection exerted by parasites and pathogens can generate a selective advantage for rare host genotypes. This mechanism, known as the Red Queen, is currently considered to be one of the most likely explanations for the predominance of sexual reproduction in natural populations. Even so, the extent to which the Red Queen can and does provide an advantage to sex in nature is fiercely debated. Here, we survey the history of the development of the Red Queen hypothesis as applied to the maintenance of sex and discuss its theoretical underpinnings. We then review and synthesize the current body of theory and empirical data relevant to assessing whether Red Queen dynamics are likely to contribute to any general explanation for why sex is so common. We conclude that while there are many independent lines of evidence in support of a role for the Red Queen, important theoretical and empirical gaps remain. In particular, there is a need for theory addressing the breadth of conditions under which the Red Queen can favor sex, predictions for the patterns of molecular evolution expected for loci under negative frequency-dependent selection, and empirical research evaluating the strength of parasite-mediated selection in nature and the genetics of susceptibility and infection.

The essence of sex in our theory is that it stores genes that are currently bad but have promise for reuse. It continually tries them in new combination, waiting for the time when the focus of disadvantage has moved elsewhere – Hamilton et al. (1990).

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Notes

  1. 1.

    Since sex and outcrossing are similar phenomena, and since Red Queen dynamics may contribute to favoring both in a similar manner, “outcrossing” is also included when “sex” is mentioned, and vice versa, unless stated otherwise.

References

  • Agrawal AF (2006) Similarity selection and the evolution of sex: revisiting the Red Queen. PLoS Biol 4: 1364–1371

    Article  CAS  Google Scholar 

  • Agrawal AF, Lively CM (2001) Parasites and the evolution of self fertilization. Evolution 55: 869–879

    Article  PubMed  CAS  Google Scholar 

  • Agrawal AF, Lively CM (2002) Infection genetics: gene-for-gene versus matching-allele models, and all points in between. Evol Ecol Res 4: 79–90

    Google Scholar 

  • Agrawal AF, Lively CM (2003) Modeling infection genetics as a two-step process combining gene-for-gene and matching-allele genetics. Proc R Soc Lond B 270: 323–334

    Article  CAS  Google Scholar 

  • Agrawal AF, Otto SP (2006) Host-parasite coevolution and selection on sex through the effects of segregation. Am Nat 168: 617–629

    Article  PubMed  Google Scholar 

  • Ameisen JC, Lelièvre JD, Pleskoff O (2002) HIV/host interactions: new lessons from the Red Queen’s country. AIDS 16: S25–S31

    Article  PubMed  Google Scholar 

  • Antonovics J, Ellstrand NC (1984) Experimental studies of the evolutionary significance of sexual reproduction. I. A test of the frequency-dependent selection hypothesis. Evolution 38: 103–115

    Article  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

    PubMed  CAS  Google Scholar 

  • Bakker EG, Toomajian C, Kreitman M, Bergelson J (2006) A genome-wide survey of R gene polymorphisms in Arabidopsis. Plant Cell 18: 1803–1818

    Article  PubMed  CAS  Google Scholar 

  • Barrett SCH, Eckert CG (1990) Variation and evolution of mating system in seed plants. In: Kawano S (ed) Biological approaches and evolutionary trends in plants. Acad Press, London, pp. 229–254

    Google Scholar 

  • Barton NH (1995) A general model for the evolution of recombination. Genet Res 65: 123–144.

    Article  PubMed  CAS  Google Scholar 

  • Barton NH, Charlesworth B (1998) Why sex and recombination? Science 281: 1985–1990

    Article  Google Scholar 

  • Bell G (1982) The masterpiece of nature. Croon Helm, London

    Google Scholar 

  • Ben-Ami F, Heller J (2005) Spatial and temporal patterns of parthenogenesis and parasitism in the freshwater snail Melanoides tuberculata. J Evol Biol 18: 138–146

    Article  PubMed  CAS  Google Scholar 

  • Ben-Ami, F, Heller J (2008) Sex versus parasitism versus density. Biol J Linn Soc 93: 527–544.

    Article  Google Scholar 

  • Bergelson J, Kreitman M, Stahl EA, Tian D (2001) Evolutionary dynamics of plant R-genes. Science 292: 2281–2285

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Bodmer WF (1972) Evolutionary significance of the HL-A system. Nature 237: 139–145

    Article  PubMed  CAS  Google Scholar 

  • Briles WE, Stone HA, Cole RK (1977) Marek’s disease: effects of B histocompatibility alloalleles in resistant and susceptible chickens. Science 195: 193–195

    Article  PubMed  CAS  Google Scholar 

  • Brown SG, Kwan S, Shero S (1995) The parasitic theory of sexual reproduction: parasitism in unisexual and bisexual geckos. Proc R Soc Lond B 260: 317–320

    Article  Google Scholar 

  • Brunet J, Mundt CC (2000) Disease, frequency-dependent selection, and genetic polymorphisms: experiments with stripe rust and wheat. Evolution 54: 406–415.

    PubMed  CAS  Google Scholar 

  • Bruvo R, Schulenburg H, Storhas M, Michiels NK (2007) Synergism between mutational meltdown and Red Queen in parthenogenetic biotypes of the freshwater planarian Schmidtea polychroa. Oikos 116: 313–323

    Article  Google Scholar 

  • Buckling A, Wei Y, Massey RC, Brockhurst MA, Hochberg ME (2006) Antagonistic coevolution with parasites increases the cost of host deleterious mutations. Proc R Soc Lond B 273: 45–49

    Article  Google Scholar 

  • Burt A (2000) Perspective: sex, recombination, and the efficacy of selection: was Weismann right? Evolution 54: 337–351

    PubMed  CAS  Google Scholar 

  • Burt A, Bell G (1987) Mammalian chiasma frequencies as a test of two theories of recombination. Nature 326: 803–805

    Article  PubMed  CAS  Google Scholar 

  • Burt A, Bell G (1991) Seed reproduction is associated with a transient escape from parasite damage in American beech. Oikos 61: 145–148

    Article  Google Scholar 

  • Busch J, Neiman M, Koslow JM (2004) Evidence for maintenance of sex by pathogens in plants. Evolution 58: 2584–2590

    PubMed  Google Scholar 

  • Carius HJ, Little TJ, Ebert D (2001) Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 55: 1136–1145

    PubMed  CAS  Google Scholar 

  • Charlesworth B (1976) Recombination modification in a fluctuating environment. Genetics 83: 181–195

    PubMed  CAS  Google Scholar 

  • Charlesworth D (2006) Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet 2: 0379–0384

    Article  CAS  Google Scholar 

  • Clarke B (1976) The ecological genetics of host-parasite relationships. In: Taylor AER, Muller R (eds) Genetic aspects of host-parasite relationships. Blackwell Scientific, Oxford, pp. 87–103

    Google Scholar 

  • Clay K, Kover PX (1996) The Red Queen hypothesis and plant/pathogen interactions. Annu Rev Phytopathol 34: 29–50

    Article  PubMed  CAS  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

    Article  Google Scholar 

  • Cooper TF, Lenski RE, Elena SF (2005) Parasites and mutational load: an experimental test of a pluralistic theory for the evolution of sex. Proc R Soc Lond B 272: 311–317

    Article  Google Scholar 

  • Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc Lond B 205: 489–511

    Article  PubMed  CAS  Google Scholar 

  • Decaestecker E, Gaba S, Raeymaekers JAM, Stocks R, Van Kerckhoven L, Ebert D, De Meester L (2007) Host-parasite ‘Red Queen’ dynamics archived in pond sediment. Nature 450: 870–873

    Article  PubMed  CAS  Google Scholar 

  • de Visser JAGM, Elena SF (2007) The evolution of sex: empirical insights into the roles of epistasis and drift. Nat Rev Genet 8: 139–149

    Article  PubMed  CAS  Google Scholar 

  • Dionne M, Miller KM, Dodson JJ, Caron F, Bernatchez L (2007) Clinal variation in MHC diversity with temperature: evidence for the role of host-pathogen interaction on local adaptation in Atlantic salmon. Evolution 61: 2154–2164

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dybdahl MF, Lively CM (1995) Host-parasite interactions: infection of common clones in natural populations of a freshwater snail (Potamopyrgus antipodarum). Proc R Soc Lond B 260: 99–103

    Article  Google Scholar 

  • Dybdahl MF, Lively CM (1998) Host-parasite coevolution: evidence for rare advantage and time-lagged selection in a natural population. Evolution 52: 1057–1066

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ellstrand NC, Antonovics J (1985) Experimental studies on the evolutionary significance of sexual reproduction. II. A test of the density-dependent selection hypothesis. Evolution 39: 657–666

    Article  Google Scholar 

  • Fischer OM, Schmid-Hempel P (2005) Selection by parasites may increase host recombination frequency. Biol Lett 1: 193–195

    Article  PubMed  CAS  Google Scholar 

  • Flor HH (1956) The complementary genic systems in flax and flax rust. Adv Genet 8: 275–296

    Google Scholar 

  • Frank SA (1992) Models of plant–pathogen coevolution. Trends Genet 8: 213–219

    PubMed  CAS  Google Scholar 

  • Frank SA (2000) Specific and non-specific defense against parasitic attack. J Theor Biol 202: 283–304

    Article  PubMed  CAS  Google Scholar 

  • Gandon S (2002) Local adaptation and the geometry of host-parasite coevolution. Ecol Lett 5: 246–256

    Article  Google Scholar 

  • Gandon S, Otto SP (2007) The evolution of sex and recombination in response to abiotic or coevolutionary fluctuations in epistasis. Genetics 175: 1835–1853

    Article  PubMed  CAS  Google Scholar 

  • Glesener RR (1979) Recombination in a simulated predator-prey interaction. Am Zool 19: 763–771

    Google Scholar 

  • Glesener RR, Tilman D (1978) Sexuality and the components of environmental uncertainty: clues from geographic parthenogenesis in terrestrial animals. Am Nat 112: 659–673

    Article  Google Scholar 

  • Greischar M, Koskella B (2007) A synthesis of experimental work on parasite local adaptation. Ecol Lett 10: 418–434

    Article  PubMed  Google Scholar 

  • Haag CR, Sakwiska O, Ebert D (2003) Test of synergistic interaction between infection and inbreeding in Daphnia magna. Evolution 57: 777–783

    PubMed  Google Scholar 

  • Hakoyama H, Nishimura T, Matsubara N, Iguchi K (2001) Difference in parasite load and nonspecific immune reaction between sexual and gynogenetic forms of Carassius auratus. Biol J Linnean Soc 72: 401–407

    Article  Google Scholar 

  • Haldane JBS (1949) Disease and evolution. Ric Sci 19 (Suppl): 68–76

    Google Scholar 

  • Hamilton WD (1980) Sex vs. non-sex vs. parasite. Oikos 35: 282–290

    Article  Google Scholar 

  • Hamilton WD (1982) Pathogens as causes of genetic diversity in their host populations, In: Anderson RM, May RM (eds) Population biology of infectious diseases. Springer, Berlin, pp. 269–296

    Google Scholar 

  • Hamilton WD, Axelrod R, Tanese R (1990) Sexual reproduction as an adaptation to resist parasites (A review). Proc Natl Acad Sci USA 87: 3566–3573

    Article  PubMed  CAS  Google Scholar 

  • Hanley KA, Bolger DT, Case TJ (1994) Comparative ecology of sexual and asexual gecko species (Lepidodactylus) in French Polynesia. Evol Ecol 8: 438–454

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Hill AVS, Yates SNR, Allsopp CM, Gupta S, Gilbert SC, Lalvani A, Aidoo M, Davenport M, Plebanski M (1994) Human leukocyte antigens and natural selection by malaria. Philos Trans R Soc Lond B 346: 379–385

    Article  CAS  Google Scholar 

  • Howard RS, Lively CM (1994) Parasitism, mutation accumulation, and the maintenance of sex. Nature 367: 554–557

    Article  PubMed  CAS  Google Scholar 

  • Howard RS, Lively CM (1998) The maintenance of sex by parasitism and mutation accumulation under epistatic fitness functions. Evolution 52: 604–610

    Article  Google Scholar 

  • Howard RS, Lively CM (2003) Opposites attract? Mate choice for parasite evasion and the evolutionary stability of sex. J Evol Biol 16: 681–689

    Article  PubMed  CAS  Google Scholar 

  • Hughes AL, Hughes MK, Howell CY, Nei M, Howard JC, Higgs P (1994) Natural selection at the class II major histocompatibility complex loci of mammals. Philos Trans R Soc Lond B 345: 359–367

    Article  Google Scholar 

  • Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167–170

    Article  PubMed  CAS  Google Scholar 

  • Hughes AL, Nei M (1989a) Evolution of the major histocompatibility complex: independent origin of non-classical class I genes in different groups of mammals. Mol Biol Evol 6: 559–579

    PubMed  CAS  Google Scholar 

  • Hughes AL, Nei M (1989b) Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci USA 86: 958–962

    Article  PubMed  CAS  Google Scholar 

  • Hughes AL, Nei M (1992) Models of host-parasite interaction and MHC polymorphism. Genetics 132: 863–864

    PubMed  CAS  Google Scholar 

  • Hughes AL, Yeager M (1998) Natural selection at major histocompatibility complex loci of vertebrates. Annu Rev Genet 32: 415–435

    Article  PubMed  CAS  Google Scholar 

  • Hutson V, Law R (1981) Evolution of recombination in populations experiencing frequency-dependent selection with time delay. Proc R Soc Lond B 213: 345–359

    Article  Google Scholar 

  • Jaenike J (1978) An hypothesis to account for the maintenance of sex within populations. Evol Theor 3: 191–194

    Google Scholar 

  • Johnson SG, Lively CM, Schrag SJ (1997) Evolution and ecological correlates of uniparental and biparental reproduction in freshwater snails, In: Streit B, Städler T, Lively CM (eds) Evolutionary ecology of freshwater animals. Birkhäuser Verlag, Basel, pp. 263–291

    Google Scholar 

  • Jokela J, Dybdahl MF, Lively CM (2009) The maintenance of sex, clonal dynamics, and host-parasite coevolution in a mixed population of sexual and asexual snails. Am Nat 174: S43–S53

    Google Scholar 

  • Jokela J, Lively CM, Dybdahl MF, Fox JA (2003) Genetic variation in sexual and clonal lineages of a freshwater snail. Biol J Linn Soc 79: 165–181

    Article  Google Scholar 

  • Jokela J, Lively CM, Fox JA, Dybdahl MF (1997) Flat reaction norms and ‘frozen’ phenotypic variation in clonal snails (Potamopyrgus antipodarum). Evolution 51: 1120–1129

    Article  Google Scholar 

  • Kelley SE (1994) Viral pathogens and the advantage of sex in the perennial Anthoxanthum odoratum. Philos Trans R Soc Lond B 346: 295–302

    Article  Google Scholar 

  • Killick SC, Carlsson AM, West SA, Little TJ (2006) Testing the pluralist approach to sex: the influence of environment on synergistic interactions between mutation load and parasitism in Daphnia magna. J Evol Biol 19(5): 1603–1611

    Article  PubMed  CAS  Google Scholar 

  • King KC, Lively CM (2009) Geographic variation in sterilizing parasite species and the Red Queen. Oikos: in press (DOI 10.1111/j.1600-0706.2009.17476.x)

    Google Scholar 

  • Knapp LA (2007) Selection on MHC? A matter of form over function. Heredity 99: 241–242

    Article  PubMed  CAS  Google Scholar 

  • Kondrashov AS (1993) Classification of hypotheses on the advantage of amphimixis. J Hered 84: 372–387

    PubMed  CAS  Google Scholar 

  • Koskella B, Lively CM (2007) Advice of the Rose: experimental coevolution of a trematode parasite and its snail host. Evolution 62: 152–159

    Article  Google Scholar 

  • Kouyos RD, Salathé M, Bonhoeffer S (2007) The Red Queen and the persistence of linkage-disequilibrium oscillations in finite and infinite populations. BMC Evol Biol 7: 211–219

    Article  PubMed  Google Scholar 

  • Kover PX, Caicedo AL (2001) The genetic architecture of disease resistance in plants and the maintenance of recombination by parasites. Mol Ecol 10: 1–16

    Article  PubMed  CAS  Google Scholar 

  • Kumpulainen T, Grapputo A, Mappes J (2004) Parasites and sexual reproduction in psychid moths. Evolution 58: 1511–1520

    PubMed  Google Scholar 

  • Lazarro BP (2005) Elevated polymorphism and divergence in the class C scavenger receptors of Drosophila melanogaster and D. simulans. Genetics 169: 2023–2034

    Article  CAS  Google Scholar 

  • Levin DA (1975) Pest pressure and recombination systems in plants. Am Nat 109: 437–451

    Article  Google Scholar 

  • Lewontin RC (1974) The genetic basis of evolutionary change. Columbia University Press, New York

    Google Scholar 

  • Lively CM (1987) Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature 328: 519–521

    Article  Google Scholar 

  • Lively CM (1992) Parthenogenesis in a freshwater snail: reproductive assurance versus parasitic release. Evolution 46: 907–913.

    Article  Google Scholar 

  • Lively CM (1996) Host-parasite coevolution and sex. Bioscience 46: 107–114

    Article  Google Scholar 

  • Lively CM (1999) Migration, virulence, and the geographic mosaic of adaptation by parasites. Am Nat 153: S34–S47

    Article  Google Scholar 

  • Lively CM (2001) Trematode infection and the distribution and dynamics of parthenogenetic snail populations. Parasitology 123: S19–S26

    Article  Google Scholar 

  • Lively CM (2006) The ecology of virulence. Ecol Lett 9: 1089–1095

    Article  PubMed  Google Scholar 

  • Lively CM, Apanius V (1995) Genetic diversity in host-parasite interactions. In: Grenfell BT, Dobson AP (eds) Ecology of infectious diseases in natural populations. Cambridge University Press, Cambridge, UK, pp. 421–449

    Chapter  Google Scholar 

  • Lively CM, Craddock C, Vrijenhoek RC (1990) The Red Queen hypothesis supported by parasitism in sexual and clonal fish. Nature 344: 864–866

    Article  Google Scholar 

  • Lively CM, Dybdahl MF (2000) Parasite adaptation to locally common host genotypes. Nature 405: 679–681

    Article  PubMed  CAS  Google Scholar 

  • Lively CM, Dybdahl MF, Jokela J, Osnas EE, Delph LF (2004) Host sex and local adaptation by parasites in a snail-trematode interaction. Am Nat 164: S6–S18

    Article  PubMed  Google Scholar 

  • Lively CM, Howard RS (1994) Selection by parasites for clonal diversity and mixed mating. Philos Trans R Soc Lond B 346: 271–281

    Article  CAS  Google Scholar 

  • Lively CM, Jokela J (1996) Clinal variation for local adaptation in a host-parasite interaction. Proc R Soc Lond B 263: 891–897

    Article  Google Scholar 

  • Lively CM, Jokela J (2002) Temporal and spatial distributions of parasites and sex in a freshwater snail. Evol Ecol Res 4: 219–226

    Google Scholar 

  • Lloyd DG (1980) Demographic factors and mating patterns in angiosperms. In: Solbrig OT (ed) Demography and evolution in plant populations. Botanical Monographs. University of California Press, Berkeley, pp. 67–88

    Google Scholar 

  • Lythgoe KA (2000) The coevolution of parasites with host-acquired immunity and the evolution of sex. Evolution 54: 1142–1156

    PubMed  CAS  Google Scholar 

  • Lythgoe KA, Read AF (1998) Catching the Red Queen? The advice of the rose. Trends Ecol Evol 13: 473–474

    Article  Google Scholar 

  • May RM, Anderson RM (1983) Epidemiology and genetics in the coevolution of parasites and hosts. Proc R Soc Lond B 219: 291–313

    Article  Google Scholar 

  • Mayer F, Brunner A (2007) Non-neutral evolution of the major histocompatibility complex class II gene DRB1 in the sac-winged bat Saccopteryx bilineata. Heredity 99: 257–264

    Article  PubMed  CAS  Google Scholar 

  • Maynard Smith J (1971) What use is sex? J Theor Biol 30: 319–355

    Article  Google Scholar 

  • Maynard Smith J (1978) The evolution of sex. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • McClelland EE, Penn DJ, Potts WK (2003) Major histocompatibility complex heterozygote superiority during coinfection. Infect Immun 71: 2079–2086

    Article  PubMed  CAS  Google Scholar 

  • Mee JA, Rowe L (2006) A comparison of parasite loads on asexual and sexual Phoxinus(Pisces: Cyprinidae). Can J Zool 84: 808–816

    Article  Google Scholar 

  • Meirmans S, Neiman M (2006) Methodologies for testing a pluralist idea for the maintenance of sex. Biol J Linn Soc 89: 605–613

    Article  Google Scholar 

  • Michiels NK, Beukeboom LW, Pongratz N, Zeitlinger J (2001) Parthenogenetic flatworms have more symbionts than their coexisting, sexual conspecifics, but does this support the Red Queen? J Evol Biol 14: 110–119

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Morand S, Manning SD, Woolhouse MEJ (1996) Parasite-host coevolution and geographic patterns of parasite infectivity and host susceptibility. Proc R Soc Lond B 263: 119–128

    Article  CAS  Google Scholar 

  • Moritz C, McCallum H, Donnellan S, Roberts JD (1991) Parasite loads in parthenogenetic and sexual lizards (Heteronotia binoei): support for the Red Queen hypothesis. Proc R Soc Lond B 244: 145–149

    Article  Google Scholar 

  • Mundt CC, Brunet J, Sackett KE (2008) Impact of density and disease on frequency-dependent selection and genetic polymorphism: experiments with stripe rust and wheat. Evol Ecol 22: 637–657.

    Article  Google Scholar 

  • Nidelet T, Kaltz O (2007) Direct and correlated responses to selection in a host-parasite system: testing for the emergence of genotype specificity. Evolution 61: 1803–1811

    Article  PubMed  Google Scholar 

  • Nordborg M, Hu TT, Ishino Y, Jhaveri J, Zheng H, Bakker E, Calabrese P, Gladstone J, Goyal R, Jakobsson M, Kim S, Morozov Y, Padhukasahasram B, Plagnol V, Rosenberg NA, Shah C, Wall JD, Wang J, Zhao K, Kalbfleisch T, Schulz V, Kreitman M, Bergelson J (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3: 1289–1299

    Article  CAS  Google Scholar 

  • Osnas EE, Lively CM (2006) Host ploidy, parasitism and immune defense in a coevolutionary snail-trematode system. J Evol Biol 19: 42–48

    Article  PubMed  CAS  Google Scholar 

  • Otto SP, Nuismer SL (2004) Species interactions and the evolution of sex. Science 304: 1018–1020

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Peters AD (1999) The effects of pathogen infection and mutation on life-history characters in Arabidopsis thaliana. J Evol Biol 12: 460–470

    Article  Google Scholar 

  • Peters AD, Lively CM (1999) The Red Queen and fluctuating epistasis: a population genetic analysis of antagonistic coevolution. Am Nat 154: 393–405

    Article  PubMed  Google Scholar 

  • Peters AD, Lively CM (2007) Short- and long-term benefits and detriments to recombination under antagonistic coevolution. J Evol Biol 20: 1206–1217

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Potts WK, Manning CJ, Wakeland EK (1994) The role of infectious disease, inbreeding and mating preferences in maintaining MHC genetic diversity: an experimental test. Philos Trans R Soc Lond B 346: 369–378

    Article  CAS  Google Scholar 

  • Price MV, Waser NM (1982) Population structure, frequency-dependent selection, and the maintenance of sexual reproduction. Evolution 36: 35–43

    Article  Google Scholar 

  • Puurtinen M, Hytönen M, Knott KE, Taskinen J, Nissinen K, Kaitala V (2004) The effects of mating system and genetic variability on susceptibility to trematode parasites in a freshwater snail, Lymnaea stagnalis. Evolution 58: 2747–2753

    PubMed  Google Scholar 

  • Rolff J, Siva-Jothy MT (2003) Invertebrate ecological immunology. Science 301: 472

    Article  PubMed  CAS  Google Scholar 

  • Ronsheim ML (1996) Evidence against a frequency-dependent advantage for sexual reproduction in Allium vineale. Am Nat 147: 718–734

    Article  Google Scholar 

  • Salathé M, Ebert D (2003) The effects of parasitism and inbreeding on the competitive ability in Daphnia magna: evidence for synergistic epistasis. J Evol Biol 16: 976–985

    Article  PubMed  Google Scholar 

  • Salathé M, Kouyos RD, Regoes RR, Bonhoeffer S (2007) Rapid parasite adaptation drives selection for high recombination rates. Evolution 62: 295–300

    Article  PubMed  Google Scholar 

  • Salathé M, Scherer A, Bonhoeffer S (2005) Neutral drift and polymorphism in gene-for-gene systems. Ecol Lett 8: 925–932

    Article  Google Scholar 

  • Schmitt J, Antonovics J (1986) Experimental studies of the evolutionary significance of sexual reproduction. VI. Effect of neighbor relatedness and aphid infestation on seedling performance. Evolution 40: 830–836

    Article  Google Scholar 

  • Schrag SJ, Mooeres AO, Ndifon GT, Read AF (1994) Ecological correlates of male outcrossing ability in a simultaneous hermaphrodite snail. Am Nat 143: 636–655

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Seger J (1988) Dynamics of some simple host parasite models with more than two genotypes in each species. Philos Trans R Soc Lond B 319: 541–555

    Article  CAS  Google Scholar 

  • Seger J, Hamilton WD (1988) Parasites and sex. In: Michod RE, Levin BR (eds) The evolution of sex. Sinauer, Sunderland, pp. 176–193

    Google Scholar 

  • Shykoff JA, Schmid-Hempel P (1991) Parasites and the advantage of genetic-variability within social insect colonies. Proc R Soc Lond B 243: 55–58

    Article  Google Scholar 

  • Slade RW, McCallum HI (1992) Overdominant vs. frequency-dependent selection at MHC loci. Genetics 132: 861–862

    PubMed  CAS  Google Scholar 

  • Stahl EA, Dwyer G, Mauricio R, Kreitman M, Bergelson J (1999) Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400: 667–671

    Article  PubMed  CAS  Google Scholar 

  • Stevens L, Yan G, Pray LA (1997) Consequences of inbreeding on invertebrate host susceptibility to parasitic infection. Evolution 51: 2032–2039

    Article  Google Scholar 

  • Strauss SY, Karban R (1994) The significance of outcrossing in an intimate plant-herbivore relationship. I. Does outcrossing provide an escape from herbivores adapted to the parent plant? Evolution 48: 454–464

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Tiffin P, Moeller DA (2006) Molecular evolution of plant immune genes. Trends Genet 22: 662–670

    Article  PubMed  CAS  Google Scholar 

  • Tiffin P, Hacker R, Gaut BS (2004) Population genetic evidence for rapid changes in intraspecific diversity and allelic cycling of a specialist defense gene in Zea. Genetics 168: 425–434

    Article  PubMed  CAS  Google Scholar 

  • Tobler M, Schlupp I (2005) Parasites in sexual and asexual mollies (Poecilia, Poeciliidae, Teleostei): a case for the Red Queen? Biol Lett 1: 166–168

    Article  PubMed  Google Scholar 

  • Todd JR, West BC, McDonald JC (1990) Human leukocyte antigen and leprosy: study in northern Louisiana and review. Rev Infect Dis 12: 63–74

    PubMed  CAS  Google Scholar 

  • Van Valen L (1973) A new evolutionary law. Evol Theor 1: 1–30

    Google Scholar 

  • Vernon JG, Okamura B, Jones CS, Noble LR (1996) Temporal patterns of clonality and parasitism in a population of freshwater bryozoans. Proc R Soc Lond B 263: 1313–1318

    Article  CAS  Google Scholar 

  • Vrijenhoek RC, Lerman S (1982) Heterozygosity and developmental stability under sexual and asexual breeding systems. Evolution 36: 768–776.

    Article  Google Scholar 

  • Webster JP, Davies CM (2001) Coevolution and compatibility in the snail-schistosome system. Parasitology 123: S41–S56

    Article  PubMed  Google Scholar 

  • Wedekind C, Walker M, Little TJ (2005) Major histocompatibility complex (MHC) effects, but no general MHC heterozygote advantage in single-strain infections. Genetics 170: 1427–1430

    Article  PubMed  CAS  Google Scholar 

  • Wegner KM, Kalbe M, Reusch TBH (2007) Innate versus adaptive immunity in sticklebacks: evidence for trade-offs from a selection experiment. J Evol Ecol 21: 473–483

    Article  Google Scholar 

  • Wegner KM, Kalbe M, Schaschl H, Reusch TBH (2004) Parasites and individual major histocompatibility complex diversity – an optimal choice? Microbes Infect 6: 1110–1116

    Article  PubMed  CAS  Google Scholar 

  • West SA, Lively CM, Read AF (1999) A pluralistic approach to sex and recombination. J Evol Biol 12: 1003–1012

    Article  Google Scholar 

  • Westerdahl H, Hansson B, Bensch S, Hasselquist D (2004) Between-year variation of MHC allele frequencies in great reed warblers: selection or drift? J Evol Biol 17: 485–492

    Article  PubMed  CAS  Google Scholar 

  • Williams GC (1966) Adaptation and natural selection. Princeton University Press, Princeton

    Google Scholar 

  • Williams GC (1975) Sex and evolution. Princeton University Press, Princeton

    Google Scholar 

  • Woolhouse MEJ, Webster JP, Domingo E, Charlesworth B, Levin BR (2002) Biological and biomedical implications of the coevolution of pathogens and their hosts. Nat Genet 32: 569–577

    Article  PubMed  CAS  Google Scholar 

  • Wuethrich B (1998) Evolution of sex: putting theory to the test. Science 281: 1980–1982

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We would like to thank P. Tiffin and D. Moeller for discussion of the molecular population genetics of disease resistance genes, J. Jokela for discussion of ploidy and susceptibility in P. antipodarum, C. Lively and D. Taylor for comments on an earlier version of the MS, and S. Bonhoeffer and an anonymous reviewer for thoughtful and helpful reviews.

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Authors and Affiliations

  1. Department of Biology, University of Iowa, 52242, Iowa City, IA, USA

    Maurine Neiman

  2. Department of Zoology, University of Oxford, Oxford, UK

    Britt Koskella

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  1. Maurine Neiman
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  2. Britt Koskella
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Correspondence to Maurine Neiman .

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Editors and Affiliations

  1. Natural Sciences, Royal Belgian Institute of, Vautierstraat 29, Bruxelles, 1000, Belgium

    Isa Schön

  2. Sciences Department of Freshwater, Royal Belgian Inst. of Natural, Vautierstraat 29, Bruxelles, 1000, Belgium

    Koen Martens

  3. Keygene N.V., Agro Business Park 90, Wageningen, 6708 PW, Netherlands

    Peter Dijk

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Neiman, M., Koskella, B. (2009). Sex and the Red Queen. In: Schön, I., Martens, K., Dijk, P. (eds) Lost Sex. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-2770-2_7

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