Red Queen Theory


The Red Queen theory was introduced to explain the apparent constancy of extinction rates. The theory states that extinction rates remain constant because taxa are in continuous evolutionary arms races with other taxa. This macroevolution version of the theory is not well supported. However, a microevolution version of the theory, in which species maintain constant levels of adaptation because of antagonistic coevolution, is well supported, especially for hosts and their parasites. The Red Queen hypothesis is now most often used to refer to the idea that host–parasite coevolution favours sexual reproduction. Meiotic recombination in hosts is proposed to generate rare genotypes, which are selectively favoured if parasites are adapted to the most common host genotypes. However, the genetic mechanism underlying the advantage of recombination in models of host–parasite coevolution is not entirely clear.

Key Concepts

  • The Red Queen theory was developed to explain the apparent constancy of extinction rates.
  • The theory proposes that continuous evolutionary arms races among species explain the constancy of extinction rates.
  • The Red Queen theory applied to macroevolution is not well supported.
  • The Red Queen theory applied to microevolution is well supported.
  • The theory is now mostly associated with the idea that host–parasite coevolution favours the evolution of sex.
  • Fluctuating fitness epistasis among genetic loci involved in the interaction between a host and its parasites may favour meiotic recombination.
  • Alternatively, recombination is favoured by selective interference among beneficial mutations in finite populations, and host–parasite coevolution maintains this interference.

Keywords: Red Queen theory; evolutionary arms race; antagonistic coevolution; host–parasite coevolution; sex; recombination

Figure 1. The proportion of taxa surviving (S) declines linearly on a log scale with taxon age (t) if the rate of extinction (μ) is constant. The equation for the line is S = eμt, with μ = 0.05 and arbitrary units for t.
Figure 2. The proportion of extinct genera decreases with genus age for marine animals over the past 541 million years (Finnegan et al., ). Finnegan, S., J. L. Payne, and S. C. Wang. 2008. The Red Queen revisited: Reevaluating the age selectivity of Phanerozoic marine genus extinctions. Paleobiology 34:318–341. Reproduced with permission.
Figure 3. The infectivity of the Daphnia host is highest with the contemporary bacterial pathogen compared to its infectivity with the pathogen from earlier and later generations (Decaestecker et al., ). Lines represent different depths (time) of pond sediment. Reproduced by permission of Springer Nature. Decaestecker, E., S. Gaba, J. A. M. Raeymaekers, R. Stoks, L. Van Kerckhoven, D. Ebert, and L. De Meester 2007.
Figure 4. A high rate of outcrossing by the nematode host was maintained only under coevolution with a highly virulent bacterium (Morran et al., ). From Morran, L. T., O. G. Schmidt, I. A. Gelarden, R. C. Parrish, and C. M. Lively. 2011. Running with the Red Queen: Host‐parasite coevolution selects for biparental sex. Science 333:216–218. Reprinted with permission from AAAS.


Abrams PA (2000) The evolution of predator–prey interactions: theory and evidence. Annual Review of Ecology and Systematics 31: 79–105.

Auld SKJR, Tinkler SK and Tinsley MC (2016) Sex as a strategy against rapidly evolving parasites. Proceedings of the Royal Society B: Biological Sciences 283 (1845 pii: 20162226).

Barton NH (1995) A general model for the evolution of recombination. Genetics Research 65: 123–144.

Barton NH (2010) Genetic linkage and natural selection. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365: 2559–2569.

Bell G (1982) The Masterpiece of Nature: The Evolution and Genetics of Sexuality. Berkeley: University of California Press.

Benton MJ (1990) Red Queen hypothesis. In: Briggs DE and Crowther PR (eds) Palaeobiology: A Synthesis, pp. 119–124. Oxford, UK: Blackwell Scientific Publications.

Best A, Ashby B, White A, et al. (2017) Host‐parasite fluctuating selection in the absence of specificity. Proceedings of the Royal Society B: Biological Sciences 284 pii: 20171615.

Darwin C (1859) On the Origin of Species by Means of Natural Selection, or, The Preservation of Favoured Races in the Struggle for Life. London: John Murray.

Decaestecker E, Gaba S, Raeymaekers JAM, et al. (2007) Host‐parasite ‘Red Queen’ dynamics archived in pond sediment. Nature 450: 870–873.

Duncan AB and Little TJ (2007) Parasite‐driven genetic change in a natural population of Daphnia. Evolution 61: 796–803.

Dybdahl MF, Jenkins CE and Nuismer SL (2014) Identifying the molecular basis of host‐parasite coevolution: merging models and mechanisms. The American Naturalist 184: 1–13.

Felsenstein J (1974) The evolutionary advantage of recombination. Genetics 78: 737–756.

Fenton A, Antonovics J and Brockhurst MA (2012) Two‐step infection processes can lead to coevolution between functionally independent infection and resistance pathways. Evolution 66: 2030–2041.

Finnegan S, Payne JL and Wang SC (2008) The Red Queen revisited: reevaluating the age selectivity of Phanerozoic marine genus extinctions. Paleobiology 34: 318–341.

Fisher RA (1930) The Genetical Theory of Natural Selection. Oxford, UK: Clarendon Press.

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

Glesener RR and Tilman D (1978) Sexuality and the components of environmental uncertainty: clues from geographic parthenogenesis in terrestrial animals. The American Naturalist 112: 659–673.

Gómez P and Buckling A (2011) Bacteria‐phage antagonistic coevolution in soil. Science 332: 106.

Hall AR, Scanlan PD, Morgan AD and Buckling A (2011) Host–parasite coevolutionary arms races give way to fluctuating selection. Ecology Letters 14: 635–642.

Hamilton WD (1980) Sex versus non‐sex versus parasite. Oikos 35: 282–290.

Hutson V and Law R (1981) Evolution of recombination in populations experiencing frequency‐dependent selection with time delay. Proceedings of the Royal Society of London. Series B: Biological Sciences 213: 345–359.

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

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

Kerstes N, Berenos C, Schmid‐Hempel P and Wegner KM (2012) Antagonistic experimental coevolution with a parasite increases host recombination frequency. BMC Evolutionary Biology 12: 18.

Laanto E, Hoikkala V, Ravantti J and Sundberg LR (2017) Long‐term genomic coevolution of host‐parasite interaction in the natural environment. Nature Communications 8: 111.

Lawlor LR and Maynard Smith J (1976) The coevolution and stability of competing species. The American Naturalist 110: 79–99.

Levin DA (1975) Pest pressure and recombination systems in plants. The American Naturalist 109: 437–451.

Lighten J, Papadopulos AST, Mohammed RS, Ward BJ, et al. (2017) Evolutionary genetics of immunological supertypes reveals two faces of the Red Queen. Nature Communications 8: 1294.

Lively CM and Howard RS (1994) Selection by parasites for clonal diversity and mixed mating. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 346: 271.

Masri L, Schulte RD, Timmermeyer N, et al. (2013) Sex differences in host defence interfere with parasite‐mediated selection for outcrossing during host–parasite coevolution. Ecology Letters 16: 461–468.

Maynard Smith J (1978) The Evolution of Sex. Cambridge, UK/New York: Cambridge University Press.

Metzger CM, Luijckx P, Bento G, Mariadassou M and Ebert D (2016) The Red Queen lives: epistasis between linked resistance loci. Evolution 70: 480–487.

Morran LT, Schmidt OG, Gelarden IA, Parrish RC and Lively CM (2011) Running with the Red Queen: host‐parasite coevolution selects for biparental sex. Science 333: 216–218.

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

Paterson S, Vogwill T, Buckling A, et al. (2010) Antagonistic coevolution accelerates molecular evolution. Nature 464: 275–278.

Peters AD and Lively CM (1999) The red queen and fluctuating epistasis: a population genetic analysis of antagonistic coevolution. The American Naturalist 154: 393–405.

Salathé M, Kouyos RD, Regoes RR and Bonhoeffer S (2008) Rapid parasite adaptation drives selection for high recombination rates. Evolution 62: 295–300.

Salathé M, Kouyos RD and Bonhoeffer S (2009) On the causes of selection for recombination underlying the Red Queen hypothesis. The American Naturalist 174: S31–S42.

Schulte RD, Makus C, Hasert B, Michiels NK and Schulenburg H (2010) Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite. Proceedings of the National Academy of Sciences 107: 7359.

da Silva J and Galbraith JD (2017) Hill–Robertson interference maintained by Red Queen dynamics favours the evolution of sex. Journal of Evolutionary Biology 30: 994–1010.

Stenseth NC and Maynard Smith J (1984) Coevolution in ecosystems: Red Queen evolution or stasis? Evolution 38: 870–880.

Tellier A, Moreno‐Gámez S and Stephan W (2014) Speed of adaptation and genomic footprints of host–parasite coevolution under arms race and trench warfare dynamics. Evolution 68: 2211–2224.

Thrall PH, Laine AL, Ravensdale M, et al. (2012) Rapid genetic change underpins antagonistic coevolution in a natural host‐pathogen metapopulation. Ecology Letters 15: 425–435.

Van Valen L (1973) A new evolutionary law. Evolutionary Theory 1: 1–30.

Venditti C, Meade A and Pagel M (2010) Phylogenies reveal new interpretation of speciation and the Red Queen. Nature 463: 349–352.

Wegner KM, Berenos C and Schmid‐Hempel P (2008) Nonadditive genetic components in resistance of the red flour beetle Tribolium castanaeum against parasite infection. Evolution 62: 2381–2392.

Wolinska J and Spaak P (2009) The cost of being common: evidence from natural Daphnia populations. Evolution 63: 1893–1901.

Woolhouse MEJ, Webster JP, Domingo E, Charlesworth B and Levin BR (2002) Biological and biomedical implications of the co‐evolution of pathogens and their hosts. Nature Genetics 32: 569.

Zliobaite I, Fortelius M and Stenseth NC (2017) Reconciling taxon senescence with the Red Queen's hypothesis. Nature 552: 92–95.

Further Reading

Benton MJ (2009) The Red Queen and the Court Jester: species diversity and the role of biotic and abiotic factors through time. Science 323: 728.

Brockhurst MA, Chapman T, King KC, et al. (2014) Running with the Red Queen: the role of biotic conflicts in evolution. Proceedings of the Royal Society B: Biological Sciences 281: 1–9.

Liow LH, Van Valen L and Stenseth NC (2011) Red Queen: from populations to taxa and communities. Trends in Ecology & Evolution 26: 349–358.

Lively CM (2010) A review of Red Queen models for the persistence of obligate sexual reproduction. Journal of Heredity 101: S13–S20.

Lively CM and Morran LT (2014) The ecology of sexual reproduction. Journal of Evolutionary Biology 27: 1292–1303.

Ridley M (1993) The Red Queen: Sex and the Evolution of Human Nature. London: Viking Press.

Salathé M, Kouyos RD and Bonhoeffer S (2008) The state of affairs in the kingdom of the Red Queen. Trends in Ecology & Evolution 23: 439–445.

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How to Cite close
da Silva, Jack(Aug 2018) Red Queen Theory. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0028127]