Red Queen

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The Red Queen hypothesis posits that sex allows hosts to evade co-evolving parasites. (Photo: William F. Duffy) From: The Red Queen Gets a New Lease on Life, Gross L. PLoS Biology Vol. 4, No. 8, e285 doi:10.1371/journal.pbio.0040285

The Red Queen's Hypothesis, Red Queen, "Red Queen's race" or "Red Queen Effect" is an evolutionary hypothesis to explain two different phenomena: the advantage of sex at the level of individuals, and the constant evolutionary arms race between competing species. In the first (microevolutionary) version, by making every individual an experiment when mixing mother's and father's genes, sex may allow a species to adapt quickly just to hold onto the ecological niche that it already has in the ecosystem. In the second (macroevolutionary) version, the probability of extinction for groups (usually families) of organisms is hypothesized to be constant within the family and random between families.

The term is taken from the Red Queen's race in Lewis Carroll's Through the Looking Glass. The Red Queen said, "It takes all the running you can do, to keep in the same place."

Arms races

Originally proposed by Leigh Van Valen (1973), the metaphor of an evolutionary arms race has been found appropriate for the descriptions of biological processes with dynamics similar to arms races. He proposed the Red Queen's Hypothesis as an explanatory tangent to his proposed Law of Extinction (also 1973) which he derived from observation of constant probabilities of extinction within families of organisms across geologic time. Put differently, Van Valen found that the ability of a family of organisms to survive does not improve over time, and that the probability of extinction for any given family is random. The Red Queen's Hypothesis as formulated by Van Valen provides a conceptual underpinning to discussions of biological evolutionary arms races, even though a direct test of the hypothesis remains elusive, particularly at the macroevolutionary level.

For example, because every improvement in one species will lead to a selective advantage for that species, variation will normally continuously lead to increases in fitness in one species or another. However, since in general different species are coevolving, improvement in one species implies that it will get a competitive advantage on the other species, and thus be able to capture a larger share of the resources available to all. This means that fitness increase in one evolutionary system will tend to lead to fitness decrease in another system. The only way that a species involved in a competition can maintain its fitness relative to the others is by in turn improving its design. (From Heylighen, 2000)

The most obvious example of this effect are the "arms races" between predators and prey (e.g. Vermeij, 1987), where the only way predators can compensate for a better defense by the prey (e.g. rabbits running faster) is by developing a better offense (e.g. foxes running faster). In this case we might consider the relative improvements (running faster) to be also absolute improvements in fitness. (From Heylighen, 2000)

It should be noted that discussions of sex and reproduction were not part of Van Valen's Red Queen's Hypothesis, which addressed evolution at scales above the species level. The microevolutionary version of the Red Queen's Hypothesis was proposed by Bell (1982), also citing Lewis Carroll, but not citing Van Valen. See below.

The paradox of sex: The "cost" of males

Science writer Matt Ridley wrote a book The Red Queen in which he discussed the debate in theoretical biology over the adaptive benefit of sexual reproduction to those species in which it appears. The connection of the Red Queen to this debate arises from the fact that the traditionally accepted theory (The Vicar of Bray) only showed adaptive benefit at the level of the species or group, not at the level of the gene. By contrast, a Red-Queen-type theory that organisms are running cyclic arms races with their parasites can explain the utility of sexual reproduction at the level of the gene by positing that the role of sex is to preserve genes which are currently disadvantageous, but which will become advantageous against the background of a likely future population of parasites.

Sex is an evolutionary puzzle. In most sexual species, males make up half the population, yet they bear no offspring directly and generally contribute little to the survival of offspring. In fact, in some species, such as lions, males pose a positive threat to live young fathered by other males (although this is simply a manifestation of Richard Dawkins' so-called selfish gene, whose goal is to reproduce itself, which may as a consequence suppress the reproduction of other genes). Obviously there are species which are exceptions to this rule, such as humans, seahorses, and penguins, amongst others. In addition, males and females must find each other to mate, and sexual selection often favors traits that reduce the survival of organisms. Thus, sexual reproduction is highly inefficient.

One possible explanation for the fact that nearly all vertebrates are sexual is that sex increases the rate at which adaptation can occur. This is for two reasons. First, if an advantageous mutation occurs in an asexual line, it is impossible for that mutation to spread without wiping out all other lines, which may have different advantageous mutations of their own. Second, it mixes up genes. Some genes might be advantageous only when paired with other genes, and sex increases the likelihood that such pairings will occur.

For sex to be advantageous for these reasons requires constant selection for changing conditions. One factor that might cause this is the constant arms race between parasites and their hosts. Parasites generally evolve quickly, due to their short lifespans. As they evolve, they attack their hosts in a variety of ways. Two consecutive generations might be faced with very different selective pressures. If this change is rapid enough, it might explain the persistence of sex.

References

  • Bell, G. (1982). The Masterpiece Of Nature: The Evolution and Genetics of Sexuality. University of California Press, Berkeley, 635 pp.
  • Lewis Carroll. 1960 (reprinted). The Annotated Alice: Alice's Adventures in Wonderland and Through the Looking-Glass, illustrated by J. Tenniel, with an Introduction and Notes by M. Gardner. The New American Library, New York, 345 pp. Through the Looking-Glass and What Alice Found There [1]
  • Dawkins, R. & Krebs, J. R. (1979). Arms races between and within species. Proceedings of the Royal society of London, B 205, 489-511.
  • F. Heylighen (2000): "The Red Queen Principle", in: F. Heylighen, C. Joslyn and V. Turchin (editors): Principia Cybernetica Web (Principia Cybernetica, Brussels), URL: http://pespmc1.vub.ac.be/REDQUEEN.html.
  • Pearson, Paul N. (2001) Red Queen hypothesis Encyclopedia of Life Sciences http://www.els.net
  • Matt Ridley (1995) The Red Queen: Sex and the Evolution of Human Nature, Penguin Books, ISBN 0-14-024548-0
  • Leigh Van Valen. (1973). "A new evolutionary law". Evolutionary Theory 1: 1—30.
  • Vermeij, G.J. (1987). Evolution and escalation: An ecological history of life. Princeton University Press, Princeton, NJ.