Red Queen's Hypothesis
Encyclopedia
The Red Queen's Hypothesis, also referred to as Red Queen, Red Queen's race or Red Queen Effect, is an evolution
ary 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 Red Queen Principle can be stated thus:
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 (microevolution
ary) version, by making every individual an experiment when mixing mother's and father's gene
s, 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 (macroevolution
ary) version, the probability of extinction for groups (usually families
) of organisms is hypothesized to be constant within the group and random among groups. Its counterpart is the Court Jester Hypothesis
, which proposes that macroevolution is driven mostly by abiotic events and forces.
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 race
s. Van Valen 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 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'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.
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. 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 vertebrate
s 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 become fixed 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. Also, in asexually reproducing organisms, especially parthenogenetic organisms, mutations conferring an advantageous allele will have to occur twice, before the advantageous allele becomes fixed in the population, resulting in a longer phase where the heterozygote for the disadvantageous allele (relative to the new advantageous allele) is fixed in the population.
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 host
s. 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.
s and immunoglobulins in the immune system
with genes coding other protein
s. The genes coding for immune system proteins evolve considerably faster.
Further evidence for the Red Queen hypothesis were 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 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 bacteria 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.
Evolution
Evolution is any change across successive generations in the heritable characteristics of biological populations. Evolutionary processes give rise to diversity at every level of biological organisation, including species, individual organisms and molecules such as DNA and proteins.Life on Earth...
ary hypothesis
Hypothesis
A hypothesis is a proposed explanation for a phenomenon. The term derives from the Greek, ὑποτιθέναι – hypotithenai meaning "to put under" or "to suppose". For a hypothesis to be put forward as a scientific hypothesis, the scientific method requires that one can test it...
. The term is taken from the Red Queen's race
Red Queen's race
The Red Queen's race is an incident that appears in Lewis Carroll's Through the Looking-Glass and involves the Red Queen, a representation of a Queen in chess, and Alice constantly running but remaining in the same spot....
in Lewis Carroll
Lewis Carroll
Charles Lutwidge Dodgson , better known by the pseudonym Lewis Carroll , was an English author, mathematician, logician, Anglican deacon and photographer. His most famous writings are Alice's Adventures in Wonderland and its sequel Through the Looking-Glass, as well as the poems "The Hunting of the...
's Through the Looking-Glass
Through the Looking-Glass
Through the Looking-Glass, and What Alice Found There is a work of literature by Lewis Carroll . It is the sequel to Alice's Adventures in Wonderland...
. The Red Queen
Red Queen (Through the Looking Glass)
The Red Queen is a fictional character in Lewis Carroll's fantasy novella, Through the Looking-Glass.- Overview :With a motif of Through the Looking-Glass being representations of the game of chess, the Red Queen could be viewed as an antagonist in the story as she is the queen for the side...
said, "It takes all the running you can do, to keep in the same place." The Red Queen Principle can be stated thus:
- In reference to an evolutionary system, continuing adaptation is needed in order for a species to maintain its relative fitness amongst the systems being co-evolved with.
The hypothesis is intended to explain two different phenomena: the advantage of sexual reproduction
Evolution of sex
The evolution of sexual reproduction is currently described by several competing scientific hypotheses. All sexually reproducing organisms derive from a common ancestor which was a single celled eukaryotic species. Many protists reproduce sexually, as do the multicellular plants, animals, and fungi...
at the level of individuals, and the constant evolutionary arms race
Evolutionary arms race
In evolutionary biology, an evolutionary arms race is an evolutionary struggle between competing sets of co-evolving genes that develop adaptations and counter-adaptations against each other, resembling an arms race, which are also examples of positive feedback...
between competing species. In the first (microevolution
Microevolution
Microevolution is the changes in allele frequencies that occur over time within a population. This change is due to four different processes: mutation, selection , gene flow, and genetic drift....
ary) version, by making every individual an experiment when mixing mother's and father's gene
Gene
A gene is a molecular unit of heredity of a living organism. It is a name given to some stretches of DNA and RNA that code for a type of protein or for an RNA chain that has a function in the organism. Living beings depend on genes, as they specify all proteins and functional RNA chains...
s, sexual reproduction
Sexual reproduction
Sexual reproduction is the creation of a new organism by combining the genetic material of two organisms. There are two main processes during sexual reproduction; they are: meiosis, involving the halving of the number of chromosomes; and fertilization, involving the fusion of two gametes and the...
may allow a species to evolve quickly just to hold onto the ecological niche
Ecological niche
In ecology, a niche is a term describing the relational position of a species or population in its ecosystem to each other; e.g. a dolphin could potentially be in another ecological niche from one that travels in a different pod if the members of these pods utilize significantly different food...
that it already occupies in the ecosystem
Ecosystem
An ecosystem is a biological environment consisting of all the organisms living in a particular area, as well as all the nonliving , physical components of the environment with which the organisms interact, such as air, soil, water and sunlight....
. In the second (macroevolution
Macroevolution
Macroevolution is evolution on a scale of separated gene pools. Macroevolutionary studies focus on change that occurs at or above the level of species, in contrast with microevolution, which refers to smaller evolutionary changes within a species or population.The process of speciation may fall...
ary) version, the probability of extinction for groups (usually families
Family (biology)
In biological classification, family is* a taxonomic rank. Other well-known ranks are life, domain, kingdom, phylum, class, order, genus, and species, with family fitting between order and genus. As for the other well-known ranks, there is the option of an immediately lower rank, indicated by the...
) of organisms is hypothesized to be constant within the group and random among groups. Its counterpart is the Court Jester Hypothesis
Court Jester Hypothesis
The Court Jester hypothesis is a term coined by University of California, Berkeley professor Anthony D. Barnosky in 1999, that describes the antithesis of the Red Queen Hypothesis in evolutionary theory...
, which proposes that macroevolution is driven mostly by abiotic events and forces.
Arms races
Leigh Van Valen
Leigh Maiorana Van Valen was an American evolutionary biologist. He was professor emeritus in the Department of Ecology and Evolution at the University of Chicago....
(1973), the metaphor of an evolutionary arms race
Evolutionary arms race
In evolutionary biology, an evolutionary arms race is an evolutionary struggle between competing sets of co-evolving genes that develop adaptations and counter-adaptations against each other, resembling an arms race, which are also examples of positive feedback...
has been found appropriate for the descriptions of biological processes with dynamics similar to arms race
Arms race
The term arms race, in its original usage, describes a competition between two or more parties for the best armed forces. Each party competes to produce larger numbers of weapons, greater armies, or superior military technology in a technological escalation...
s. Van Valen 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
Extinction
In biology and ecology, extinction is the end of an organism or of a group of organisms , normally a species. The moment of extinction is generally considered to be the death of the last individual of the species, although the capacity to breed and recover may have been lost before this point...
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
Testability
Testability, a property applying to an empirical hypothesis, involves two components: the logical property that is variously described as contingency, defeasibility, or falsifiability, which means that counterexamples to the hypothesis are logically possible, and the practical feasibility of...
of the hypothesis remains elusive, particularly at the macroevolutionary level. This concept remains similar to that of a system obeying a self-organized criticality
Self-organized criticality
In physics, self-organized criticality is a property of dynamical systems which have a critical point as an attractor. Their macroscopic behaviour thus displays the spatial and/or temporal scale-invariance characteristic of the critical point of a phase transition, but without the need to tune...
.
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
Competition (biology)
Competition is an interaction between organisms or species, in which the fitness of one is lowered by the presence of another. Limited supply of at least one resource used by both is required. Competition both within and between species is an important topic in ecology, especially community ecology...
for resources can maintain its fitness relative to other competing species is by improving its specific
Species
In biology, a species is one of the basic units of biological classification and a taxonomic rank. A species is often defined as a group of organisms capable of interbreeding and producing fertile offspring. While in many cases this definition is adequate, more precise or differing measures are...
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'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 RidleyMatt Ridley
Matthew White Ridley, FRSL, FMedSci is an English journalist, writer, biologist, and businessman.-Career:...
popularized the term "the red queen" in connection with sexual selection
Sexual selection
Sexual selection, a concept introduced by Charles Darwin in his 1859 book On the Origin of Species, is a significant element of his theory of natural selection...
in his book The Red Queen. In the book, Ridley discussed the debate in theoretical biology over the adaptive benefit of sexual reproduction
Sexual reproduction
Sexual reproduction is the creation of a new organism by combining the genetic material of two organisms. There are two main processes during sexual reproduction; they are: meiosis, involving the halving of the number of chromosomes; and fertilization, involving the fusion of two gametes and the...
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
Vicar of Bray (scientific hypothesis)
The "Vicar of Bray" is the name given to a hypothesis attempting to explain why sexual reproduction might be favoured over asexual reproduction, in which sexual populations are able to outcompete asexual populations because they evolve more rapidly in response to environmental changes...
) only showed adaptive benefit at the level of the species or group, not at the level of the gene
Gene
A gene is a molecular unit of heredity of a living organism. It is a name given to some stretches of DNA and RNA that code for a type of protein or for an RNA chain that has a function in the organism. Living beings depend on genes, as they specify all proteins and functional RNA chains...
(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
Sex ratio
Sex ratio is the ratio of males to females in a population. The primary sex ratio is the ratio at the time of conception, secondary sex ratio is the ratio at time of birth, and tertiary sex ratio is the ratio of mature organisms....
, yet they bear no offspring
Offspring
In biology, offspring is the product of reproduction, of a new organism produced by one or more parents.Collective offspring may be known as a brood or progeny in a more general way...
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
Infanticide (zoology)
In animals, infanticide involves the killing of young offspring by a mature animal of its own species, and is studied in zoology, specifically in the field of ethology. Ovicide is the analogous destruction of eggs. Although human infanticide has been widely studied, the practice has been observed...
fathered by other males. In addition, males and females must spend resources to attract and compete for mates. Sexual selection
Sexual selection
Sexual selection, a concept introduced by Charles Darwin in his 1859 book On the Origin of Species, is a significant element of his theory of natural 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
Handicap principle
The handicap principle is a hypothesis originally proposed in 1975 by biologist Amotz Zahavi to explain how evolution may lead to "honest" or reliable signaling between animals who have an obvious motivation to bluff or deceive each other...
for more on this). Thus, sexual reproduction can be highly inefficient.
One possible explanation for the fact that nearly all vertebrate
Vertebrate
Vertebrates are animals that are members of the subphylum Vertebrata . Vertebrates are the largest group of chordates, with currently about 58,000 species described. Vertebrates include the jawless fishes, bony fishes, sharks and rays, amphibians, reptiles, mammals, and birds...
s are sexual is that sex increases the rate at which adaptation can occur. This is for two reasons. Firstly, if an advantageous mutation
Mutation
In molecular biology and genetics, mutations are changes in a genomic sequence: the DNA sequence of a cell's genome or the DNA or RNA sequence of a virus. They can be defined as sudden and spontaneous changes in the cell. Mutations are caused by radiation, viruses, transposons and mutagenic...
occurs in an asexual
Asexual reproduction
Asexual reproduction is a mode of reproduction by which offspring arise from a single parent, and inherit the genes of that parent only, it is reproduction which does not involve meiosis, ploidy reduction, or fertilization. A more stringent definition is agamogenesis which is reproduction without...
line, it is impossible for that mutation to become fixed 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. Also, in asexually reproducing organisms, especially parthenogenetic organisms, mutations conferring an advantageous allele will have to occur twice, before the advantageous allele becomes fixed in the population, resulting in a longer phase where the heterozygote for the disadvantageous allele (relative to the new advantageous allele) is fixed in the population.
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 host
Host (biology)
In biology, a host is an organism that harbors a parasite, or a mutual or commensal symbiont, typically providing nourishment and shelter. In botany, a host plant is one that supplies food resources and substrate for certain insects or other fauna...
s. 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.
Observational evidence
Evidence for this explanation for the evolution of sex is provided by comparison of the rate of molecular evolution of genes for kinaseKinase
In chemistry and biochemistry, a kinase is a type of enzyme that transfers phosphate groups from high-energy donor molecules, such as ATP, to specific substrates, a process referred to as phosphorylation. Kinases are part of the larger family of phosphotransferases...
s and immunoglobulins in the immune system
Immune system
An immune system is a system of biological structures and processes within an organism that protects against disease by identifying and killing pathogens and tumor cells. It detects a wide variety of agents, from viruses to parasitic worms, and needs to distinguish them from the organism's own...
with genes coding other protein
Protein
Proteins are biochemical compounds consisting of one or more polypeptides typically folded into a globular or fibrous form, facilitating a biological function. A polypeptide is a single linear polymer chain of amino acids bonded together by peptide bonds between the carboxyl and amino groups of...
s. The genes coding for immune system proteins evolve considerably faster.
Further evidence for the Red Queen hypothesis were 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 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 bacteria 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.
See also
- Evolutionary arms raceEvolutionary arms raceIn evolutionary biology, an evolutionary arms race is an evolutionary struggle between competing sets of co-evolving genes that develop adaptations and counter-adaptations against each other, resembling an arms race, which are also examples of positive feedback...
- Chaos theoryChaos theoryChaos theory is a field of study in mathematics, with applications in several disciplines including physics, economics, biology, and philosophy. Chaos theory studies the behavior of dynamical systems that are highly sensitive to initial conditions, an effect which is popularly referred to as the...
- Punctuated equilibriumPunctuated equilibriumPunctuated equilibrium is a theory in evolutionary biology which proposes that most species will exhibit little net evolutionary change for most of their geological history, remaining in an extended state called stasis...
- Self-organized criticalitySelf-organized criticalityIn physics, self-organized criticality is a property of dynamical systems which have a critical point as an attractor. Their macroscopic behaviour thus displays the spatial and/or temporal scale-invariance characteristic of the critical point of a phase transition, but without the need to tune...
Further reading
- Bell, G. (1982). The Masterpiece Of Nature: The Evolution and Genetics of Sexuality. University of California Press, Berkeley, 378 pp.
- Dawkins, R.Richard DawkinsClinton Richard Dawkins, FRS, FRSL , known as Richard Dawkins, is a British ethologist, evolutionary biologist and author...
& Krebs, J. R. (1979). Arms races between and within species. Proceedings of the Royal society of London, B 205, 489-511. - Francis HeylighenFrancis HeylighenFrancis Paul Heylighen is a Belgian cyberneticist, and research professor at the Vrije Universiteit Brussel, the Dutch-speaking Free University of Brussels, where he directs the transdisciplinary research group on "Evolution, Complexity and Cognition".-Biography:Francis Heylighen was born on...
(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 SciencesEncyclopedia of Life SciencesThe Encyclopedia of Life Sciences is an encyclopedia that spans the entire spectrum of life sciences and is published by Wiley-Blackwell....
http://www.els.net - Ridley, M.Matt RidleyMatthew White Ridley, FRSL, FMedSci is an English journalist, writer, biologist, and businessman.-Career:...
(1995) The Red Queen: Sex and the Evolution of Human Nature, Penguin Books, ISBN 0-14-024548-0 - Leigh Van ValenLeigh Van ValenLeigh Maiorana Van Valen was an American evolutionary biologist. He was professor emeritus in the Department of Ecology and Evolution at the University of Chicago....
. (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.