Red Queen hypothesis  

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Kunstformen der Natur (1904) by Ernst Haeckel
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Kunstformen der Natur (1904) by Ernst Haeckel

The Red Queen's Hypothesis, Red Queen, "Red Queen's race" or "Red Queen Effect" is an evolutionary hypothesis. 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."

The hypothesis is intended to explain two different phenomena: the advantage of sexual reproduction 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, sexual reproduction may allow a species to evolve quickly just to hold onto the ecological niche that it already occupies 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 group and random among groups.

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 geological 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 evolutionary arms races, even though a direct test of the hypothesis remains elusive, particularly at the macroevolutionary level. This concept remains similar to that of a system obeying a self-organized criticality.

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 co-evolving, improvement in one species implies that it will get a competitive advantage over 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 for resources can maintain its fitness relative to other competing species is by improving its specific fitness. (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)

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 popularized the term "the red queen" in connection with sexual selection in his book The Red Queen. In the book, Ridley 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 (Vicar of Bray) only showed adaptive benefit at the level of the species or group, not at the level of the gene (although, it must be added here that the protean 'Vicar of Bray' adaptation is very useful to some species that belong to the lower levels of the food chain). 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 that are currently disadvantageous, but that 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 could be viewed as 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). In addition, males and females must spend resources to attract and compete for mates. Sexual selection also can favor traits that reduce the fitness of an organism, such as brightly colored plumage in birds of paradise that increases the likelihood for an individual to be noticed by both predators and potential mates (see the handicap principle for more on this). Thus, sexual reproduction can be 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. Firstly, 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. Secondly, it mixes up alleles. Some instances of genetic variation might be advantageous only when paired with other mutations, 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 because of their short life cycles. 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.

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