Red Queen hypothesis

Etymology

The phenomenon's name is derived from a statement that the Red Queen made to Alice in Lewis Carroll's Through the Looking-Glass in her explanation of the nature of Looking-Glass Land:

Now, here, you see, it takes all the running you can do, to keep in the same place.

Van Valen coined the hypothesis "Red Queen" because under this interpretation where species have to "run" or evolve in order to stay in the same place or remain extant.

Leigh Van Valen (1973) proposed the metaphor of an evolutionary arms race, which was appropriate for the description of biological processes with dynamics similar to arms races. In respective processes, an adaptation in a population of one species (e.g., predators, parasites) may change the selection pressure on a population of another species (e.g., prey, host), giving rise to an antagonistic coevolution.

Interspecies arms race:

"The rabbit runs faster than the fox, because the rabbit is running for his life while the fox is only running for his dinner." Aesop

The emergence of the concept and illustrations of it

Van Valen proposed the Red Queen 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 lack of correlation between age and extinction is suggestive of a random process. The Red Queen 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 different species tend to co-evolve, an 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 the fitness increase in one evolutionary system will tend to lead to the 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 than their parents) is by developing a better offense (e.g.. foxes running faster than their parents). In this case, we might consider the relative improvements (rabbits running faster than foxes or vice versa) to be also absolute improvements in fitness. (From Heylighen, 2000)

Discussions of sex and reproduction were not part of Van Valen's Red Queen hypothesis, which addressed evolution at scales above the species level. The microevolutionary version of the Red Queen hypothesis was proposed by Bell (1982), also citing Lewis Carroll, but not citing Van Valen (see below).

Application to human conflict

One can apply such arms races to human conflict and interpret them as a prominent cause of conflict. According to Azar Gat, the Red Queen effect arises when two competing groups find themselves in a security dilemma. The security dilemma results when a group takes defensive measures (which possess inherent offensive capabilities) to improve their security, triggering a military arms race. This arms race, much like the example previously referenced, causes each side to consume ever increasing amounts of resources in order to outpace the other and to gain an advantage. If an advantage is gained, the arms race is over and the group with more resources has won. However, typically both sides continue to match each other stride for stride, thus triggering the Red Queen effect, as no matter how many resources each side invests, neither is able to gain an advantage. The situation somewhat resembles the prisoner's dilemma. Neither side can stop the arms race, due to mutual suspicion and fears that the other group will gain a significant tactical advantage. Because of this, the Red Queen effect is a common outcome of inter-human competition and conflict.

The paradox of sex: The "cost" of males

Science writer Matt Ridley popularized the term in connection with sexual selection in his 1993 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 Vicar of Bray hypothesis only showed adaptive benefit at the level of the species or group, not at the level of the gene (although 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 thesis 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.

Further evidence was observed of the Red Queen to see allelic affects under sexual selection. The Red Queen Hypothesis leads to the understanding that allelic recombination is advantageous for populations that engage in aggressive biotic interactions, such as predator-host interactions. In cases of predator-host relations, sexual reproduction can quicken the production of new multi-locus genotypes allowing the host to escape invasion by parasites that have adapted to the prior generations of typical hosts. Mutational effects can be represented by models to describe how recombination through sexual reproduction can be advantageous. According to the mutational deterministic hypothesis, if the deleterious mutation rate is high, and if those mutations interact to cause a general decline in organismal fitness, then sexual reproduction provides an advantage over asexually reproducing organisms by allowing populations to eliminate the deleterious mutations not only more rapidly, but also most effectively. Recombination is one of the fundamental means that explain why many organisms have evolved to reproduce sexually.

Sexual organisms must spend resources to find mates. In the case of sexual dimorphism, usually only one of the sexes contributes to the survival of their offspring. In such cases, the only adaptive benefit of having a second sex is the capability of sexual selection, by which organisms can improve their genotype. In this way, sexual reproduction can be highly inefficient.

Observational evidence

Evidence for this explanation for the evolution of sex is provided by the comparison of the rate of molecular evolution of genes for kinases and immunoglobulins in the immune system with genes coding other proteins. The genes coding for immune system proteins evolve considerably faster.

Further evidence for the Red Queen hypothesis was provided by observing long‐term dynamics and parasite coevolution in a mixed sexual and asexual population of snails (Potamopyrgus antipodarum). The number of sexuals, the number of asexuals, and the rates of parasite infection for both were monitored. It was found that clones that were plentiful at the beginning of the study became more susceptible to parasites over time. As parasite infections increased, the once-plentiful clones dwindled dramatically in number. Some clonal types disappeared entirely. Meanwhile, sexual snail populations remained much more stable over time.

In 2011, researchers used the microscopic roundworm Caenorhabditis elegans as a host and the pathogenic bacterium Serratia marcescens to generate a host–parasite coevolutionary system in a controlled environment, allowing them to conduct more than 70 evolution experiments testing the Red Queen hypothesis. They genetically manipulated the mating system of C. elegans, causing populations to mate either sexually, by self-fertilization, or a mixture of both within the same population. Then they exposed those populations to the S. marcescens parasite. It was found that the self-fertilizing populations of C. elegans were rapidly driven extinct by the coevolving parasites, while sex allowed populations to keep pace with their parasites, a result consistent with the Red Queen hypothesis.

Does the Red Queen hypothesis explain how sex is maintained?

Critics of the Red Queen hypothesis for the maintenance of sex question whether the constantly changing interaction of hosts and their parasites is sufficiently common to provide the principal explanation for the evolution of sex. In particular, Otto and Nuismer presented results showing that species interactions (e.g. host vs parasite interactions) typically select against sex. They concluded that although the Red Queen process favors sex under certain circumstances, it alone does not account for sex. Otto and Gerstein further stated "it seems doubtful to us that strong selection per gene is sufficiently commonplace for the Red Queen hypothesis to explain the ubiquity of sex."

Parker reviewed numerous genetic studies on plant disease resistance and failed to uncover a single example consistent with the assumptions of the Red Queen hypothesis.

Hanley et al. studied mite infestations of parthenogenetic gecko species and its two related sexual ancestral species. Contrary to expectation based on the Red Queen hypothesis, they found that the prevalence, abundance and mean intensity of mites in sexual geckos was significantly higher than in asexuals sharing the same habitat.

In a study of the coevolution of the red flour beetle, Tribolium castaneum with its natural microsporidian parasite Nosema whitei, Greef and Schmid-Hempel found no effect of the parasite on the beetle’s recombination rate after eight generations.

Weeks evaluated the Red queen model for the maintenance of sex in a clonal-sexual fish complex (Poeciliidae: Poeciliopsis). They found that parasite intensity was not correlated with clonal frequency as assumed by the Red Queen model, and concluded that this model is unlikely to maintain sex in this clonal-sexual complex.

Tobler and Schlupp tested the prediction of the Red Queen hypothesis that asexual lineages should suffer from a higher parasitic load if they coexist with closely related sexuals. This prediction was tested using four populations of the sexual fish species Poecilia latipinna and its asexual relative Poecilia Formosa. Contrary to expectation, no differences in parasitic load could be detected between the two species.

Currently, there is no consensus among biologists on the main selective forces maintaining sex. The competing models to explain the adaptive function of sex have been reviewed by Birdsell and Wills.

Historical studies

The influence of heterogeneity in species genomes has been recognized and studied since the time of Darwin (1876) in the areas of heterosis (hybrid vigor), inbreeding and genetic deterioration, operating on the theory that lessening of the choice of gene variants and of potential cooperation among different gene types limits the capabilities of the restricted organism. Resultant genetic drift or genetic isolates reduce available corresponding genetic material volumes, where variable limitations can catalyze a consequential population bottleneck.

A study published in 2013 in Science which examined the history of groups of extinct mammals illustrates failure to adapt and evolve new species when confronted by a deteriorating environment. An interesting insight can be obtained from physical research.

Evolution of aging

The Red Queen hypothesis has been also invoked by some authors to explain evolution of aging. The main idea is that aging is favored by natural selection since it allows faster adaptation to changing conditions, especially in order to keep pace with the evolution of pathogens, predators and prey.

Court jester hypothesis

A competing evolutionary idea is the court jester hypothesis, which indicates that an arms race is not the driving force of evolution on a large scale, but rather it is abiotic factors.