Red Queen hypothesis
The Red Queen hypothesis is a hypothesis in evolutionary biology proposed in 1973, that species must constantly adapt, evolve, and proliferate in order to survive while pitted against ever-evolving opposing species. The hypothesis was intended to explain the constant extinction probability as observed in the paleontological record caused by co-evolution between competing species; however, it has also been suggested that the Red Queen hypothesis explains the advantage of sexual reproduction at the level of individuals, and the positive correlation between speciation and extinction rates in most higher taxa.
Origin
In 1973, Leigh Van Valen proposed the hypothesis as an "explanatory tangent" to explain the "law of extinction" known as "Van Valen's law", which states that the probability of extinction does not depend on the lifetime of the species or higher-rank taxon, instead being constant over millions of years for any given taxon. However, the probability of extinction is strongly related to adaptive zones, because different taxa have different probabilities of extinction. In other words, extinction of a species occurs randomly with respect to age, but nonrandomly with respect to ecology. Collectively, these two observations suggest that the effective environment of any homogeneous group of organisms deteriorates at a stochastically constant rate. Van Valen proposed that this is the result of an evolutionary zero-sum game driven by interspecific competition: the evolutionary progress of one species deteriorates the fitness of coexisting species, but because coexisting species evolve as well, no one species gains a long-term increase in fitness, and the overall fitness of the system remains constant.Van Valen named the hypothesis "Red Queen" because under his hypothesis, species have to "run" or evolve in order to stay in the same place, or else go extinct. As the Red Queen said to Alice in Lewis Carroll's Through the Looking-Glass in her explanation of the nature of Looking-Glass Land:
Examples
Positive correlation between speciation and extinction rates (Stanley's rule)
Palaeontological data suggest that high speciation rates correlate with high extinction rates in almost all major taxa. This correlation has been attributed to a number of ecological factors, but it may result also from a Red Queen situation, in which each speciation event in a clade deteriorates the fitness of coexisting species in the same clade.Evolution of sex
Discussions of the evolution of sex 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, also citing Lewis Carroll, but not citing Van Valen.The Red Queen hypothesis is used independently by Hartung and Bell to explain the evolution of sex, by John Jaenike to explain the maintenance of sex and W. D. Hamilton to explain the role of sex in response to parasites. In all cases, sexual reproduction confers species variability and a faster generational response to selection by making offspring genetically unique. Sexual species are able to improve their genotype in changing conditions. Consequently, co-evolutionary interactions, between host and parasite, for example, may select for sexual reproduction in hosts in order to reduce the risk of infection. Oscillations in genotype frequencies are observed between parasites and hosts in an antagonistic coevolutionary way without necessitating changes to the phenotype. In multi-host and multi-parasite coevolution, the Red Queen dynamics could affect what host and parasite types will become dominant or rare. 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. By contrast, a Red-Queen-type thesis suggesting that organisms are running 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.
However, the assumption of the Red Queen hypothesis, that the primary factor in maintaining sexual reproduction is the generation of genetic variation does not appear to be generally applicable. Ruderfer et al. analyzed the ancestry of strains of the yeasts Saccharomyces cerevisiae and Saccharomyces paradoxus under natural conditions and concluded that outcrossing occurs only about once every 50,000 cell divisions. This low frequency of outcrossing implies that there is little opportunity for the production of recombinational variation. In nature, mating is likely most often between closely related yeast cells. Mating occurs when haploid cells of opposite mating type MATa and MATα come into contact, and Ruderfer et al. pointed out that such contacts are frequent between closely related yeast cells for two reasons. The first is that cells of opposite mating type are present together in the same ascus, the sac that contains the cells directly produced by a single meiosis, and these cells can mate with each other. The second reason is that haploid cells of one mating type, upon cell division, often produce cells of the opposite mating type with which they can mate. The relative rarity in nature of meiotic events that result from outcrossing is inconsistent with the idea that production of genetic variation is the main selective force maintaining meiosis in this organism. However, these findings in yeast are consistent with the alternative idea that the main selective force maintaining meiosis is enhanced recombinational repair of DNA damage, since this benefit is realized during each meiosis, whether or not out-crossing occurs.
Further evidence of the Red Queen hypothesis was observed in allelic effects 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–prey or parasite–host interactions. In cases of parasite-host relations, sexual reproduction can quicken the production of new multi-locus genotypes allowing the host to escape 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 one of the sexes contributes more to the survival of their offspring. In such cases, the only adaptive benefit of having a second sex is the possibility of sexual selection, by which organisms can improve their genotype.
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. The number of sexuals, the number of asexuals, and the rates of parasitic 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.
On the other hand, Hanley et al. studied mite infestations of a 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. Critics of the Red Queen hypothesis question whether the constantly changing environment of hosts and parasites is sufficiently common to explain the evolution of sexual reproduction. In particular, Otto and Nuismer presented findings showing that species interactions usually select against sexual reproduction. They concluded that, even though the Red Queen hypothesis favors sex under certain circumstances, it alone does not account for the ubiquity of sex. Otto and Gerstein further stated that "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.
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. However, a study of the frequency of outcrossing in natural populations showed that self-fertilization is the predominant mode of reproduction in C. elegans, with infrequent outcrossing events occurring at a rate of around 1%. Although meioses that result in selfing are unlikely to contribute significantly to beneficial genetic variability, these meioses may provide the adaptive benefit of recombinational repair of DNA damages that arise, especially under stressful conditions.
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.