Red Queen Theory

Abstract

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.
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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.

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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. http://www.els.net [doi: 10.1002/9780470015902.a0028127]