Gene-centered view of evolution

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With gene defined as "not just one single physical bit of DNA [but] all replicas of a particular bit of DNA distributed throughout the world", the gene-centered view of evolution, gene's eye view, gene selection theory, or selfish gene theory holds that adaptive evolution occurs through the differential survival of competing genes, increasing the allele frequency of those alleles whose phenotypic trait effects successfully promote their own propagation. The proponents of this viewpoint argue that, since heritable information is passed from generation to generation almost exclusively by DNA, natural selection and evolution are best considered from the perspective of genes.

Proponents of the gene-centered viewpoint argue that it permits understanding of diverse phenomena such as altruism and intragenomic conflict that are otherwise difficult to explain from an organism-centered viewpoint.

The gene-centered view of evolution is a synthesis of the theory of evolution by natural selection, the particulate inheritance theory, and the non-transmission of acquired characters. It states that those alleles whose phenotypic effects successfully promote their own propagation will be favorably selected relative to their competitor alleles within the population. This process produces adaptations for the benefit of alleles that promote the reproductive success of the organism, or of other organisms containing the same allele (kin altruism and green-beard effects), or even its own propagation relative to the other genes within the same organism (selfish genes and intragenomic conflict).

Overview

John Maynard Smith

 

Richard Dawkins

The gene-centered view of evolution is a model for the evolution of social characteristics such as selfishness and altruism.

Acquired characteristics

The formulation of the central dogma of molecular biology was summarized by Maynard Smith:

If the central dogma is true, and if it is also true that nucleic acids are the only means whereby information is transmitted between generations, this has crucial implications for evolution. It would imply that all evolutionary novelty requires changes in nucleic acids, and that these changes – mutations – are essentially accidental and non-adaptive in nature. Changes elsewhere – in the egg cytoplasm, in materials transmitted through the placenta, in the mother's milk – might alter the development of the child, but, unless the changes were in nucleic acids, they would have no long-term evolutionary effects.

— Maynard Smith

The rejection of the inheritance of acquired characters, combined with Ronald Fisher the statistician, giving the subject a mathematical footing, and showing how Mendelian genetics was compatible with natural selection in his 1930 book The Genetical Theory of Natural Selection. J. B. S. Haldane, and Sewall Wright, paved the way to the formulation of the selfish-gene theory. For cases where environment can influence heredity, see epigenetics.

The gene as the unit of selection

The view of the gene as the unit of selection was developed mainly in the works of Richard Dawkins, W. D. Hamilton, Colin Pittendrigh and George C. Williams. It was mainly popularized and expanded by Dawkins in his book The Selfish Gene (1976).

According to Williams' 1966 book Adaptation and Natural Selection,

[t]he essence of the genetical theory of natural selection is a statistical bias in the relative rates of survival of alternatives (genes, individuals, etc.). The effectiveness of such bias in producing adaptation is contingent on the maintenance of certain quantitative relationships among the operative factors. One necessary condition is that the selected entity must have a high degree of permanence and a low rate of endogenous change, relative to the degree of bias (differences in selection coefficients).

— Williams, 1966, pp. 22–23

Williams argued that "[t]he natural selection of phenotypes cannot in itself produce cumulative change, because phenotypes are extremely temporary manifestations." Each phenotype is the unique product of the interaction between genome and environment. It does not matter how fit and fertile a phenotype is, it will eventually be destroyed and will never be duplicated.

Since 1954, it has been known that DNA is the main physical substrate to genetic information, and it is capable of high-fidelity replication through many generations. So, a particular gene coded in a nucleobase sequence of a lineage of replicated DNA molecules can have a high permanence and a low rate of endogenous change.

In normal sexual reproduction, an entire genome is the unique combination of father's and mother's chromosomes produced at the moment of fertilization. It is generally destroyed with its organism, because "meiosis and recombination destroy genotypes as surely as death." Only half of it is transmitted to each descendant due to independent segregation.

And the high prevalence of horizontal gene transfer in bacteria and archaea means that genomic combinations of these asexually reproducing groups are also transient in evolutionary time: "The traditional view, that prokaryotic evolution can be understood primarily in terms of clonal divergence and periodic selection, must be augmented to embrace gene exchange as a creative force."

The gene as an informational entity persists for an evolutionarily significant span of time through a lineage of many physical copies.

In his book River out of Eden, Dawkins coins the phrase God's utility function to explain his view on genes as units of selection. He uses this phrase as a synonym of the "meaning of life" or the "purpose of life". By rephrasing the word purpose in terms of what economists call a utility function, meaning "that which is maximized", Dawkins attempts to reverse-engineer the purpose in the mind of the Divine Engineer of Nature, or the utility function of god. Finally, Dawkins argues that it is a mistake to assume that an ecosystem or a species as a whole exists for a purpose. He writes that it is incorrect to suppose that individual organisms lead a meaningful life either; in nature, only genes have a utility function – to perpetuate their own existence with indifference to great sufferings inflicted upon the organisms they build, exploit and discard.

Organisms as vehicles

Genes are usually packed together inside a genome, which is itself contained inside an organism. Genes group together into genomes because "genetic replication makes use of energy and substrates that are supplied by the metabolic economy in much greater quantities than would be possible without a genetic division of labour." They build vehicles to promote their mutual interests of jumping into the next generation of vehicles. As Dawkins puts it, organisms are the "survival machines" of genes.

The phenotypic effect of a particular gene is contingent on its environment, including the fellow genes constituting with it the total genome. A gene never has a fixed effect, so how is it possible to speak of a gene for long legs? It is because of the phenotypic differences between alleles. One may say that one allele, all other things being equal or varying within certain limits, causes greater legs than its alternative. This difference enables the scrutiny of natural selection.

"A gene can have multiple phenotypic effects, each of which may be of positive, negative or neutral value. It is the net selective value of a gene's phenotypic effect that determines the fate of the gene." For instance, a gene can cause its bearer to have greater reproductive success at a young age, but also cause a greater likelihood of death at a later age. If the benefit outweighs the harm, averaged out over the individuals and environments in which the gene happens to occur, then phenotypes containing the gene will generally be positively selected and thus the abundance of that gene in the population will increase.

Even so, it becomes necessary to model the genes in combination with their vehicle as well as in combination with the vehicle's environment.

Selfish-gene theory

The selfish-gene theory of natural selection can be restated as follows:

Genes do not present themselves naked to the scrutiny of natural selection, instead they present their phenotypic effects. [...] Differences in genes give rise to differences in these phenotypic effects. Natural selection acts on the phenotypic differences and thereby on genes. Thus genes come to be represented in successive generations in proportion to the selective value of their phenotypic effects.

— Cronin, 1991, p. 60

The result is that "the prevalent genes in a sexual population must be those that, as a mean condition, through a large number of genotypes in a large number of situations, have had the most favourable phenotypic effects for their own replication." In other words, we expect selfish genes ("selfish" meaning that it promotes its own survival without necessarily promoting the survival of the organism, group or even species). This theory implies that adaptations are the phenotypic effects of genes to maximize their representation in future generations. An adaptation is maintained by selection if it promotes genetic survival directly, or else some subordinate goal that ultimately contributes to successful reproduction.

Individual altruism and genetic egoism

The gene is a unit of hereditary information that exists in many physical copies in the world, and which particular physical copy will be replicated and originate new copies does not matter from the gene's point of view. A selfish gene could be favored by selection by producing altruism among organisms containing it. The idea is summarized as follows:

If a gene copy confers a benefit B on another vehicle at cost C to its own vehicle, its costly action is strategically beneficial if pB > C, where p is the probability that a copy of the gene is present in the vehicle that benefits. Actions with substantial costs therefore require significant values of p. Two kinds of factors ensure high values of p: relatedness (kinship) and recognition (green beards).

— Haig, 1997, p. 288

A gene in a somatic cell of an individual may forgo replication to promote the transmission of its copies in the germ line cells. It ensures the high value of p = 1 due to their constant contact and their common origin from the zygote.

The kin selection theory predicts that a gene may promote the recognition of kinship by historical continuity: a mammalian mother learns to identify her own offspring in the act of giving birth; a male preferentially directs resources to the offspring of mothers with whom he has copulated; the other chicks in a nest are siblings; and so on. The expected altruism between kin is calibrated by the value of p, also known as the coefficient of relatedness. For instance, an individual has a p = 1/2 in relation to his brother, and p = 1/8 to his cousin, so we would expect, ceteris paribus, greater altruism among brothers than among cousins. In this vein, geneticist J. B. S. Haldane famously joked, "Would I lay down my life to save my brother? No, but I would to save two brothers or eight cousins." However, examining the human propensity for altruism, kin selection theory seems incapable of explaining cross-familiar, cross-racial and even cross-species acts of kindness.

Green-beard effect

Green-beard effects gained their name from a thought-experiment first presented by Bill Hamilton and then popularized and given its current name by Richard Dawkins who considered the possibility of a gene that caused its possessors to develop a green beard and to be nice to other green-bearded individuals. Since then, "green-beard effect" has come to refer to forms of genetic self-recognition in which a gene in one individual might direct benefits to other individuals that possess the gene. Such genes would be especially selfish, benefiting themselves regardless of the fates of their vehicles. Since then, green-beard genes have been discovered in nature, such as Gp-9 in fire ants (Solenopsis invicta), csA in social amoeba (Dictyostelium discoideum), and FLO1 in budding yeast (Saccharomyces cerevisiae).

Intragenomic conflict

Main article: Intragenomic conflict

As genes are capable of producing individual altruism, they are capable of producing conflict among genes inside the genome of one individual. This phenomenon is called intragenomic conflict and arises when one gene promotes its own replication in detriment to other genes in the genome. The classic example is segregation distorter genes that cheat during meiosis or gametogenesis and end up in more than half of the functional gametes. These genes can persist in a population even when their transmission results in reduced fertility. Egbert Leigh compared the genome to "a parliament of genes: each acts in its own self-interest, but if its acts hurt the others, they will combine together to suppress it" to explain the relative low occurrence of intragenomic conflict.

Price equation

Main article: Price equation

The Price equation is a covariance equation that is a mathematical description of evolution and natural selection. The Price equation was derived by George R. Price, working in London to rederive W. D. Hamilton's work on kin selection.

Advocates

Besides Richard Dawkins and George C. Williams, other biologists and philosophers have expanded and refined the selfish-gene theory, such as John Maynard Smith, George R. Price, Robert Trivers, David Haig, Helena Cronin, David Hull, Philip Kitcher, and Daniel C. Dennett.

Criticisms

The gene-centric view has been opposed by Ernst Mayr, Stephen Jay Gould, David Sloan Wilson, and philosopher Elliott Sober. An alternative, multilevel selection (MLS), has been advocated by E. O. Wilson, David Sloan Wilson, Sober, Richard E. Michod, and Samir Okasha.

Writing in the New York Review of Books, Gould has characterized the gene-centered perspective as confusing book-keeping with causality. Gould views selection as working on many levels, and has called attention to a hierarchical perspective of selection. Gould also called the claims of Selfish Gene "strict adaptationism", "ultra-Darwinism", and "Darwinian fundamentalism", describing them as excessively "reductionist". He saw the theory as leading to a simplistic "algorithmic" theory of evolution, or even to the re-introduction of a teleological principle. Mayr went so far as to say "Dawkins' basic theory of the gene being the object of evolution is totally non-Darwinian."

Gould also addressed the issue of selfish genes in his essay "Caring groups and selfish genes". Gould acknowledged that Dawkins was not imputing conscious action to genes, but simply using a shorthand metaphor commonly found in evolutionary writings. To Gould, the fatal flaw was that "no matter how much power Dawkins wishes to assign to genes, there is one thing that he cannot give them – direct visibility to natural selection." Rather, the unit of selection is the phenotype, not the genotype, because it is phenotypes that interact with the environment at the natural-selection interface. So, in Kim Sterelny's summation of Gould's view, "gene differences do not cause evolutionary changes in populations, they register those changes." Richard Dawkins replied to this criticism in a later book, The Extended Phenotype, that Gould confused particulate genetics with particulate embryology, stating that genes do "blend", as far as their effects on developing phenotypes are concerned, but that they do not blend as they replicate and recombine down the generations.

Since Gould's death in 2002, Niles Eldredge has continued with counter-arguments to gene-centered natural selection. Eldredge notes that in Dawkins' book A Devil's Chaplain, which was published just before Eldredge's book, "Richard Dawkins comments on what he sees as the main difference between his position and that of the late Stephen Jay Gould. He concludes that it is his own vision that genes play a causal role in evolution," while Gould (and Eldredge) "sees genes as passive recorders of what worked better than what".

 

Group selection

From Wikipedia, the free encyclopedia

https://en.wikipedia.org/wiki/Group_selection 

 

Early explanations of social behaviour, such as the lekking of blackcock, spoke of "the good of the species". Blackcocks at the Lek watercolour and bodycolour by Archibald Thorburn, 1901.

Group selection is a proposed mechanism of evolution in which natural selection acts at the level of the group, instead of at the more conventional level of the individual.

Early authors such as V. C. Wynne-Edwards and Konrad Lorenz argued that the behavior of animals could affect their survival and reproduction as groups, speaking for instance of actions for the good of the species. In the 1930s, R.A. Fisher and J.B.S. Haldane proposed the concept of kin selection, a form of altruism from the gene-centered view of evolution, arguing that animals should sacrifice for their relatives, and thereby implying that they should not sacrifice for non-relatives. From the mid 1960s, evolutionary biologists such as John Maynard Smith, W. D. Hamilton, George C. Williams, and Richard Dawkins argued that natural selection acted primarily at the level of the individual. They argued on the basis of mathematical models that individuals would not altruistically sacrifice fitness for the sake of a group. They persuaded the majority of biologists that group selection did not occur, other than in special situations such as the haplodiploid social insects like honeybees (in the Hymenoptera), where kin selection was possible.

In 1994 David Sloan Wilson and Elliott Sober argued for multi-level selection, including group selection, on the grounds that groups, like individuals, could compete. In 2010 three authors including E. O. Wilson, known for his work on social insects especially ants, again revisited the arguments for group selection. They argued that group selection can occur when competition between two or more groups, some containing altruistic individuals who act cooperatively together, is more important for survival than competition between individuals within each group, provoking a strong rebuttal from a large group of evolutionary biologists and behavior analysts.

Early developments

Further information: natural selection and kin selection

Charles Darwin developed the theory of evolution in his book, Origin of Species. Darwin also made the first suggestion of group selection in The Descent of Man that the evolution of groups could affect the survival of individuals. He wrote, "If one man in a tribe... invented a new snare or weapon, the tribe would increase in number, spread, and supplant other tribes. In a tribe thus rendered more numerous there would always be a rather better chance of the birth of other superior and inventive members."

Once Darwinism had been accepted in the modern synthesis of the mid-twentieth century, animal behavior was glibly explained with unsubstantiated hypotheses about survival value, which was largely taken for granted. The naturalist Konrad Lorenz had argued loosely in books like On Aggression (1966) that animal behavior patterns were "for the good of the species", without actually studying survival value in the field. Richard Dawkins noted that Lorenz was a "'good of the species' man" so accustomed to group selection thinking that he did not realize his views "contravened orthodox Darwinian theory". The ethologist Niko Tinbergen praised Lorenz for his interest in the survival value of behavior, and naturalists enjoyed Lorenz's writings for the same reason. In 1962, group selection was used as a popular explanation for adaptation by the zoologist V. C. Wynne-Edwards. In 1976, Richard Dawkins wrote a well-known book on the importance of evolution at the level of the gene or the individual, The Selfish Gene.

Social behavior in honeybees is explained by kin selection: their haplodiploid inheritance system makes workers very closely related to their queen (centre).

From the mid 1960s, evolutionary biologists argued that natural selection acted primarily at the level of the individual. In 1964, John Maynard Smith, C. M. Perrins (1964), and George C. Williams in his 1966 book Adaptation and Natural Selection cast serious doubt on group selection as a major mechanism of evolution; Williams's 1971 book Group Selection assembled writings from many authors on the same theme.

It was at that time generally agreed that the primary exception of social group selection was in the social insects, and the explanation was limited to the unique inheritance system (involving haplodiploidy) of the eusocial Hymenoptera such as honeybees, which encourages kin selection, since workers are closely related.

Kin selection and inclusive fitness theory

Further information: Kin selection and inclusive fitness

Experiments from the late 1970s suggested that selection involving groups was possible. Early group selection models assumed that genes acted independently, for example a gene that coded for cooperation or altruism. Genetically-based reproduction of individuals implies that, in group formation, the altruistic genes would need a way to act for the benefit of members in the group to enhance the fitness of many individuals with the same gene. But it is expected from this model that individuals of the same species would compete against each other for the same resources. This would put cooperating individuals at a disadvantage, making genes for cooperation likely to be eliminated. Group selection on the level of the species is flawed because it is difficult to see how selective pressures would be applied to competing/non-cooperating individuals.

Kin selection between related individuals is accepted as an explanation of altruistic behavior. R.A. Fisher in 1930 and J.B.S. Haldane in 1932 set out the mathematics of kin selection, with Haldane famously joking that he would willingly die for two brothers or eight cousins. In this model, genetically related individuals cooperate because survival advantages to one individual also benefit kin who share some fraction of the same genes, giving a mechanism for favoring genetic selection.

Inclusive fitness theory, first proposed by W. D. Hamilton in the early 1960s, gives a selection criterion for evolution of social traits when social behavior is costly to an individual organism's survival and reproduction. The criterion is that the reproductive benefit to relatives who carry the social trait, multiplied by their relatedness (the probability that they share the altruistic trait) exceeds the cost to the individual. Inclusive fitness theory is a general treatment of the statistical probabilities of social traits accruing to any other organisms likely to propagate a copy of the same social trait. Kin selection theory treats the narrower but simpler case of the benefits to close genetic relatives (or what biologists call 'kin') who may also carry and propagate the trait. A significant group of biologists support inclusive fitness as the explanation for social behavior in a wide range of species, as supported by experimental data. An article was published in Nature with over a hundred coauthors.

One of the questions about kin selection is the requirement that individuals must know if other individuals are related to them, or kin recognition. Any altruistic act has to preserve similar genes. One argument given by Hamilton is that many individuals operate in "viscous" conditions, so that they live in physical proximity to relatives. Under these conditions, they can act altruistically to any other individual, and it is likely that the other individual will be related. This population structure builds a continuum between individual selection, kin selection, kin group selection and group selection without a clear boundary for each level. However, early theoretical models by D.S. Wilson et al. and Taylor showed that pure population viscosity cannot lead to cooperation and altruism. This is because any benefit generated by kin cooperation is exactly cancelled out by kin competition; additional offspring from cooperation are eliminated by local competition. Mitteldorf and D. S. Wilson later showed that if the population is allowed to fluctuate, then local populations can temporarily store the benefit of local cooperation and promote the evolution of cooperation and altruism. By assuming individual differences in adaptations, Yang further showed that the benefit of local altruism can be stored in the form of offspring quality and thus promote the evolution of altruism even if the population does not fluctuate. This is because local competition among more individuals resulting from local altruism increases the average local fitness of the individuals that survive.

Another explanation for the recognition of genes for altruism is that a single trait, group reciprocal kindness, is capable of explaining the vast majority of altruism that is generally accepted as "good" by modern societies. The phenotype of altruism relies on recognition of the altruistic behavior by itself. The trait of kindness will be recognized by sufficiently intelligent and undeceived organisms in other individuals with the same trait. Moreover, the existence of such a trait predicts a tendency for kindness to unrelated organisms that are apparently kind, even if the organisms are of another species. The gene need not be exactly the same, so long as the effect or phenotype is similar. Multiple versions of the gene—or even meme—would have virtually the same effect. This explanation was given by Richard Dawkins as an analogy of a man with a green beard. Green-bearded men are imagined as tending to cooperate with each other simply by seeing a green beard, where the green beard trait is incidentally linked to the reciprocal kindness trait.

Multilevel selection theory

Further information: Unit of selection

Kin selection or inclusive fitness is accepted as an explanation for cooperative behavior in many species, but there are some species, including some human behavior, that are difficult to explain with only this approach. In particular, it does not seem to explain the rapid rise of human civilization. David Sloan Wilson has argued that other factors must also be considered in evolution. Wilson and others have continued to develop group selection models.

Early group selection models were flawed because they assumed that genes acted independently; but genetically-based interactions among individuals are ubiquitous in group formation because genes must cooperate for the benefit of association in groups to enhance the fitness of group members. Additionally, group selection on the level of the species is flawed because it is difficult to see how selective pressures would be applied; selection in social species of groups against other groups, rather than the species entire, seems to be the level at which selective pressures are plausible. On the other hand, kin selection is accepted as an explanation of altruistic behavior. Some biologists argue that kin selection and multilevel selection are both needed to "obtain a complete understanding of the evolution of a social behavior system".

In 1994 David Sloan Wilson and Elliott Sober argued that the case against group selection had been overstated. They considered whether groups can have functional organization in the same way as individuals, and consequently whether groups can be "vehicles" for selection. They do not posit evolution on the level of the species, but selective pressures that winnow out small groups within a species, e.g. groups of social insects or primates. Groups that cooperate better might survive and reproduce more than those that did not. Resurrected in this way, Wilson & Sober's new group selection is called multilevel selection theory.

In 2010, Martin Nowak, C. E. Tarnita and E. O. Wilson argued for multi-level selection, including group selection, to correct what they saw as deficits in the explanatory power of inclusive fitness. A response from 137 other evolutionary biologists argued "that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature".

David Sloan Wilson and Elliott Sober's 1994 Multilevel Selection Model, illustrated by a nested set of Russian matryoshka dolls. Wilson himself compared his model to such a set.

Wilson compared the layers of competition and evolution to nested sets of Russian matryoshka dolls. The lowest level is the genes, next come the cells, then the organism level and finally the groups. The different levels function cohesively to maximize fitness, or reproductive success. The theory asserts that selection for the group level, involving competition between groups, must outweigh the individual level, involving individuals competing within a group, for a group-benefiting trait to spread.

Multilevel selection theory focuses on the phenotype because it looks at the levels that selection directly acts upon. For humans, social norms can be argued to reduce individual level variation and competition, thus shifting selection to the group level. The assumption is that variation between different groups is larger than variation within groups. Competition and selection can operate at all levels regardless of scale. Wilson wrote, "At all scales, there must be mechanisms that coordinate the right kinds of action and prevent disruptive forms of self-serving behavior at lower levels of social organization." E. O. Wilson summarized, "In a group, selfish individuals beat altruistic individuals. But, groups of altruistic individuals beat groups of selfish individuals."

Wilson ties the multilevel selection theory regarding humans to another theory, gene-culture coevolution, by acknowledging that culture seems to characterize a group-level mechanism for human groups to adapt to environmental changes.

MLS theory can be used to evaluate the balance between group selection and individual selection in specific cases. An experiment by William Muir compared egg productivity in hens, showing that a hyper-aggressive strain had been produced through individual selection, leading to many fatal attacks after only six generations; by implication, it could be argued that group selection must have been acting to prevent this in real life. Group selection has most often been postulated in humans and, notably, eusocial Hymenoptera that make cooperation a driving force of their adaptations over time and have a unique system of inheritance involving haplodiploidy that allows the colony to function as an individual while only the queen reproduces.

Wilson and Sober's work revived interest in multilevel selection. In a 2005 article, E. O. Wilson argued that kin selection could no longer be thought of as underlying the evolution of extreme sociality, for two reasons. First, he suggested, the argument that haplodiploid inheritance (as in the Hymenoptera) creates a strong selection pressure towards nonreproductive castes is mathematically flawed. Second, eusociality no longer seems to be confined to the hymenopterans; increasing numbers of highly social taxa have been found in the years since Wilson's foundational text Sociobiology: A New Synthesis was published in 1975. These including a variety of insect species, as well as two rodent species (the naked mole-rat and the Damaraland mole rat). Wilson suggests the equation for Hamilton's rule:

rb > c

(where b represents the benefit to the recipient of altruism, c the cost to the altruist, and r their degree of relatedness) should be replaced by the more general equation

rb_k + b_e > c

in which b_k is the benefit to kin (b in the original equation) and b_e is the benefit accruing to the group as a whole. He then argues that, in the present state of the evidence in relation to social insects, it appears that b_e>rb_k, so that altruism needs to be explained in terms of selection at the colony level rather than at the kin level. However, kin selection and group selection are not distinct processes, and the effects of multi-level selection are already accounted for in Hamilton's rule, rb>c, provided that an expanded definition of r, not requiring Hamilton's original assumption of direct genealogical relatedness, is used, as proposed by E. O. Wilson himself.

Spatial populations of predators and prey show restraint of reproduction at equilibrium, both individually and through social communication, as originally proposed by Wynne-Edwards. While these spatial populations do not have well-defined groups for group selection, the local spatial interactions of organisms in transient groups are sufficient to lead to a kind of multi-level selection. There is however as yet no evidence that these processes operate in the situations where Wynne-Edwards posited them.

Rauch et al.'s analysis of host-parasite evolution is broadly hostile to group selection. Specifically, the parasites do not individually moderate their transmission; rather, more transmissible variants – which have a short-term but unsustainable advantage – arise, increase, and go extinct.

Applications

Differing evolutionarily stable strategies

Further information: Evolutionarily stable strategy

The problem with group selection is that for a whole group to get a single trait, it must spread through the whole group first by regular evolution. But, as J. L. Mackie suggested, when there are many different groups, each with a different evolutionarily stable strategy, there is selection between the different strategies, since some are worse than others. For example, a group where altruism was universal would indeed outcompete a group where every creature acted in its own interest, so group selection might seem feasible; but a mixed group of altruists and non-altruists would be vulnerable to cheating by non-altruists within the group, so group selection would collapse.

Implications in population biology

Social behaviors such as altruism and group relationships can impact many aspects of population dynamics, such as intraspecific competition and interspecific interactions. In 1871, Darwin argued that group selection occurs when the benefits of cooperation or altruism between subpopulations are greater than the individual benefits of egotism within a subpopulation. This supports the idea of multilevel selection, but kinship also plays an integral role because many subpopulations are composed of closely related individuals. An example of this can be found in lions, which are simultaneously cooperative and territorial. Within a pride, males protect the pride from outside males, and females, who are commonly sisters, communally raise cubs and hunt. However, this cooperation seems to be density dependent. When resources are limited, group selection favors prides that work together to hunt. When prey is abundant, cooperation is no longer beneficial enough to outweigh the disadvantages of altruism, and hunting is no longer cooperative.

Interactions between different species can also be affected by multilevel selection. Predator-prey relationships can also be affected. Individuals of certain monkey species howl to warn the group of the approach of a predator. The evolution of this trait benefits the group by providing protection, but could be disadvantageous to the individual if the howling draws the predator's attention to them. By affecting these interspecific interactions, multilevel and kinship selection can change the population dynamics of an ecosystem.

Multilevel selection attempts to explain the evolution of altruistic behavior in terms of quantitative genetics. Increased frequency or fixation of altruistic alleles can be accomplished through kin selection, in which individuals engage in altruistic behavior to promote the fitness of genetically similar individuals such as siblings. However, this can lead to inbreeding depression, which typically lowers the overall fitness of a population. However, if altruism were to be selected for through an emphasis on benefit to the group as opposed to relatedness and benefit to kin, both the altruistic trait and genetic diversity could be preserved. However, relatedness should still remain a key consideration in studies of multilevel selection. Experimentally imposed multilevel selection on Japanese quail was more effective by an order of magnitude on closely related kin groups than on randomized groups of individuals.

Gene-culture coevolution in humans

Main articles: Dual inheritance theory and cultural group selection

 

Humanity has developed extremely rapidly, arguably through gene-culture coevolution, leading to complex cultural artefacts like the gopuram of the Sri Mariammam temple, Singapore.

Gene-culture coevolution (also called dual inheritance theory) is a modern hypothesis (applicable mostly to humans) that combines evolutionary biology and modern sociobiology to indicate group selection. It treats culture as a separate evolutionary system that acts in parallel to the usual genetic evolution to transform human traits. It is believed that this approach of combining genetic influence with cultural influence over several generations is not present in the other hypotheses such as reciprocal altruism and kin selection, making gene-culture evolution one of the strongest realistic hypotheses for group selection. Fehr provides evidence of group selection taking place in humans presently with experimentation through logic games such as prisoner's dilemma, the type of thinking that humans have developed many generations ago.

Gene-culture coevolution allows humans to develop highly distinct adaptations to the local pressures and environments more quickly than with genetic evolution alone. Robert Boyd and Peter J. Richerson, two strong proponents of cultural evolution, postulate that the act of social learning, or learning in a group as done in group selection, allows human populations to accrue information over many generations. This leads to cultural evolution of behaviors and technology alongside genetic evolution. Boyd and Richerson believe that the ability to collaborate evolved during the Middle Pleistocene, a million years ago, in response to a rapidly changing climate.

In 2003, the behavioral scientist Herbert Gintis examined cultural evolution statistically, offering evidence that societies that promote pro-social norms have higher survival rates than societies that do not. Gintis wrote that genetic and cultural evolution can work together. Genes transfer information in DNA, and cultures transfer information encoded in brains, artifacts, or documents. Language, tools, lethal weapons, fire, cooking, etc., have a long-term effect on genetics. For example, cooking led to a reduction of size of the human gut, since less digestion is needed for cooked food. Language led to a change in the human larynx and an increase in brain size. Projectile weapons led to changes in human hands and shoulders, such that humans are much better at throwing objects than the closest human relative, the chimpanzee.

Behaviour

In 2019, Howard Rachlin and colleagues proposed group selection of behavioural patterns, such as learned altruism, during ontogeny parallel to group selection during phylogeny.

Criticism

The use of the Price equation to support group selection was challenged by van Veelen in 2012, arguing that it is based on invalid mathematical assumptions.

Richard Dawkins and other advocates of the gene-centered view of evolution remain unconvinced about group selection. In particular, Dawkins suggests that group selection fails to make an appropriate distinction between replicators and vehicles.

The psychologist Steven Pinker concluded that "group selection has no useful role to play in psychology or social science", since it "is not a precise implementation of the theory of natural selection, as it is, say, in genetic algorithms or artificial life simulations. Instead it is a loose metaphor, more like the struggle among kinds of tires or telephones."

The evolutionary biologist Jerry Coyne summarized the arguments in The New York Review of Books in non-technical terms as follows:

Group selection isn't widely accepted by evolutionists for several reasons. First, it's not an efficient way to select for traits, like altruistic behavior, that are supposed to be detrimental to the individual but good for the group. Groups divide to form other groups much less often than organisms reproduce to form other organisms, so group selection for altruism would be unlikely to override the tendency of each group to quickly lose its altruists through natural selection favoring cheaters. Further, little evidence exists that selection on groups has promoted the evolution of any trait. Finally, other, more plausible evolutionary forces, like direct selection on individuals for reciprocal support, could have made humans prosocial. These reasons explain why only a few biologists, like [David Sloan] Wilson and E. O. Wilson (no relation), advocate group selection as the evolutionary source of cooperation.

 

Eusociality

From Wikipedia, the free encyclopedia

https://en.wikipedia.org/wiki/Eusociality 

 

Co-operative brood rearing, seen here in honeybees, is a condition of eusociality.

Eusociality (from Greek εὖ eu "good" and social), the highest level of organization of sociality, is defined by the following characteristics: cooperative brood care (including care of offspring from other individuals), overlapping generations within a colony of adults, and a division of labor into reproductive and non-reproductive groups. The division of labor creates specialized behavioral groups within an animal society which are sometimes referred to as 'castes'. Eusociality is distinguished from all other social systems because individuals of at least one caste usually lose the ability to perform at least one behavior characteristic of individuals in another caste.

Eusociality exists in certain insects, crustaceans and mammals. It is mostly observed and studied in the Hymenoptera (ants, bees, and wasps) and in Isoptera (termites). A colony has caste differences: queens and reproductive males take the roles of the sole reproducers, while soldiers and workers work together to create a living situation favorable for the brood. In addition to Hymenoptera and Isoptera, there are two known eusocial vertebrates among rodents: the naked mole-rat and the Damaraland mole-rat. Some shrimp, such as Synalpheus regalis, are also eusocial. E. O. Wilson and others have claimed that humans have evolved a weak form of eusociality, but these arguments have been disputed.

History

The term "eusocial" was introduced in 1966 by Suzanne Batra, who used it to describe nesting behavior in Halictine bees. Batra observed the cooperative behavior of the bees, males and females alike, as they took responsibility for at least one duty (i.e., burrowing, cell construction, oviposition) within the colony. The cooperativeness was essential as the activity of one labor division greatly influenced the activity of another.

For example, the size of pollen balls, a source of food, depended on when the egg-laying females oviposited. If the provisioning by pollen collectors was incomplete by the time the egg-laying female occupied a cell and oviposited, the size of the pollen balls would be small, leading to small offspring. Batra applied this term to species in which a colony is started by a single individual. Batra described other species, wherein the founder is accompanied by numerous helpers—as in a swarm of bees or ants—as "hypersocial".

In 1969, Charles D. Michener further expanded Batra's classification with his comparative study of social behavior in bees. He observed multiple species of bees (Apoidea) in order to investigate the different levels of animal sociality, all of which are different stages that a colony may pass through. Eusociality, which is the highest level of animal sociality a species can attain, specifically had three characteristics that distinguished it from the other levels:

1. "Egg-layers and worker-like individuals among adult females" (division of labor)
2. The overlap of generations (mother and adult offspring)
3. Cooperative work on the cells of the bees' honeycomb

Weaver ants, here collaborating to pull nest leaves together, can be considered eusocial, as they have a permanent division of labor.

E. O. Wilson then extended the terminology to include other social insects, such as ants, wasps, and termites. Originally, it was defined to include organisms (only invertebrates) that had the following three features:

1. Reproductive division of labor (with or without sterile castes)
2. Overlapping generations
3. Cooperative care of young

As eusociality became a recognized widespread phenomenon, however, it was also discovered in a group of chordates, the mole-rats. Further research also distinguished another possibly important criterion for eusociality known as "the point of no return". This is characterized by eusocial individuals that become fixed into one behavioral group, which usually occurs before reproductive maturity. This prevents them from transitioning between behavioral groups and creates an animal society that is truly dependent on each other for survival and reproductive success. For many insects, this irreversibility has changed the anatomy of the worker caste, which is sterile and provides support for the reproductive caste.

Taxonomic range

Most eusocial societies exist in arthropods, while a few are found in mammals. Ferns may exhibit eusocial behavior amongst clones.

In insects

A swarming meat-eater ant colony

 

See also: Sexual selection in social insects and Identity in social insects

The order Hymenoptera contains the largest group of eusocial insects, including ants, bees, and wasps—those with reproductive "queens" and more or less sterile "workers" and/or "soldiers" that perform specialized tasks. For example, in the well-studied social wasp Polistes versicolor, dominant females perform tasks such as building new cells and ovipositing, while subordinate females tend to perform tasks like feeding the larvae and foraging. The task differentiation between castes can be seen in the fact that subordinates complete 81.4% of the total foraging activity, while dominants only complete 18.6% of the total foraging. Eusocial species with a sterile caste are sometimes called hypersocial.

While only a moderate percentage of species in bees (families Apidae and Halictidae) and wasps (Crabronidae and Vespidae) are eusocial, nearly all species of ants (Formicidae) are eusocial. Some major lineages of wasps are mostly or entirely eusocial, including the subfamilies Polistinae and Vespinae. The corbiculate bees (subfamily Apinae of family Apidae) contain four tribes of varying degrees of sociality: the highly eusocial Apini (honey bees) and Meliponini (stingless bees), primitively eusocial Bombini (bumble bees), and the mostly solitary or weakly social Euglossini (orchid bees). Eusociality in these families is sometimes managed by a set of pheromones that alter the behavior of specific castes in the colony. These pheromones may act across different species, as observed in Apis andreniformis (black dwarf honey bee), where worker bees responded to queen pheromone from the related Apis florea (red dwarf honey bee). Pheromones are sometimes used in these castes to assist with foraging. Workers of the Australian stingless bee Tetragonula carbonaria, for instance, mark food sources with a pheromone, helping their nest mates to find the food.

Reproductive specialization generally involves the production of sterile members of the species, which carry out specialized tasks to care for the reproductive members. It can manifest in the appearance of individuals within a group whose behavior or morphology is modified for group defense, including self-sacrificing behavior ("altruism"). An example of a species whose sterile caste displays this altruistic behavior is Myrmecocystus mexicanus, one of the species of honey ant. Select sterile workers fill their abdomens with liquid food until they become immobile and hang from the ceilings of the underground nests, acting as food storage for the rest of the colony. Not all social species of insects have distinct morphological differences between castes. For example, in the Neotropical social wasp Synoeca surinama, social displays determine the caste ranks of individuals in the developing brood. These castes are sometimes further specialized in their behavior based on age. For example, Scaptotrigona postica workers assume different roles in the nest based on their age. Between approximately 0–40 days old, the workers perform tasks within the nest such as provisioning cell broods, colony cleaning, and nectar reception and dehydration. Once older than 40 days, Scaptotrigona postica workers move outside of the nest to practice colony defense and foraging.

In Lasioglossum aeneiventre, a halictid bee from Central America, nests may be headed by more than one female; such nests have more cells, and the number of active cells per female is correlated with the number of females in the nest, implying that having more females leads to more efficient building and provisioning of cells. In similar species with only one queen, such as Lasioglossum malachurum in Europe, the degree of eusociality depends on the clime in which the species is found.

Termites (order Blattodea, infraorder Isoptera) make up another large portion of highly advanced eusocial animals. The colony is differentiated into various castes: the queen and king are the sole reproducing individuals; workers forage and maintain food and resources; and soldiers defend the colony against ant attacks. The latter two castes, which are sterile and perform highly specialized, complex social behaviors, are derived from different stages of pluripotent larvae produced by the reproductive caste. Some soldiers have jaws so enlarged (specialized for defense and attack) that they are unable to feed themselves and must be fed by workers.

Austroplatypus incompertus is a species of ambrosia beetle native to Australia, and is the first beetle (order Coleoptera) to be recognized as eusocial. This species forms colonies in which a single female is fertilized, and is protected by many unfertilized females, which also serve as workers excavating tunnels in trees. This species also participates in cooperative brood care, in which individuals care for juveniles that are not their own.

Some species of gall-inducing insects, including the gall-forming aphid, Pemphigus spyrothecae (order Hemiptera), and thrips such as Kladothrips (order Thysanoptera), are also described as eusocial. These species have very high relatedness among individuals due to their partially asexual mode of reproduction (sterile soldier castes being clones of the reproducing female), but the gall-inhabiting behavior gives these species a defensible resource that sets them apart from related species with similar genetics. They produce soldier castes capable of fortress defense and protection of their colony against both predators and competitors. In these groups, therefore, high relatedness alone does not lead to the evolution of social behavior, but requires that groups occur in a restricted, shared area. These species have morphologically distinct soldier castes that defend against kleptoparasites (parasitism by theft) and are able to reproduce parthenogenetically (without fertilization).

In crustaceans

Eusociality has also arisen in three different lineages among some crustaceans that live in separate colonies. Synalpheus regalis, Synalpheus filidigitus, Synalpheus elizabethae, Synalpheus chacei, Synalpheus riosi, Synalpheus duffyi, Synalpheus microneptunus, and Synalpheus cayoneptunus are the eight recorded species of parasitic shrimp that rely on fortress defense and live in groups of closely related individuals in tropical reefs and sponges, living eusocially with a typically a single breeding female and a large number of male defenders, armed with enlarged snapping claws. As with other eusocial societies, there is a single shared living space for the colony members, and the non-breeding members act to defend it.

The fortress defense hypothesis additionally points out that because sponges provide both food and shelter, there is an aggregation of relatives (because the shrimp do not have to disperse to find food), and much competition for those nesting sites. Being the target of attack promotes a good defense system (soldier caste); soldiers therefore promote the fitness of the whole nest by ensuring safety and reproduction of the queen.

Eusociality offers a competitive advantage in shrimp populations. Eusocial species were found to be more abundant, occupy more of the habitat, and use more of the available resources than non-eusocial species. Other studies add to these findings by pointing out that cohabitation was more rare than expected by chance, and that most sponges were dominated by one species, which was frequently eusocial.

In nonhuman mammals

Naked mole-rat, one of two eusocial species in the Bathyergidae

Among mammals, eusociality is known in two species in the Bathyergidae, the naked mole-rat (Heterocephalus glaber) and the Damaraland mole-rat (Fukomys damarensis), both of which are highly inbred. Usually living in harsh or limiting environments, these mole-rats aid in raising siblings and relatives born to a single reproductive queen. However, this classification is controversial owing to disputed definitions of 'eusociality'. To avoid inbreeding, mole rats sometimes outbreed and establish new colonies when resources are sufficient. Most of the individuals cooperatively care for the brood of a single reproductive female (the queen) to which they are most likely related. Thus, it is uncertain whether mole rats classify as true eusocial organisms, since their social behavior depends largely on their resources and environment.

Some mammals in the Carnivora and Primates exhibit eusocial tendencies, especially meerkats (Suricata suricatta) and dwarf mongooses (Helogale parvula). These show cooperative breeding and marked reproductive skews. In the dwarf mongoose, the breeding pair receives food priority and protection from subordinates and rarely has to defend against predators.

In humans

Further information: Group selection

An early 21st century debate focused on whether humans are prosocial or eusocial. Edward O. Wilson called humans eusocial apes, arguing for similarities to ants, and observing that early hominins cooperated to rear their children while other members of the same group hunted and foraged. Wilson argued that through cooperation and teamwork, ants and humans form superorganisms. Wilson's claims were vigorously rejected, not only because they were based on group selection, but also because human reproductive labor is not divided between castes. However, it has been claimed that suicide, male homosexuality, and female menopause evolved through kin selection, which, if true, would by some definitions make humans eusocial.

Evolution

Main article: Evolution of eusociality

Phylogenetic distribution

Eusociality is a rare but widespread phenomenon in species in at least seven orders in the animal kingdom, as shown in the phylogenetic tree (non-eusocial groups not shown). All species of termites are eusocial, and it is believed that they were the first eusocial animals to evolve, sometime in the upper Jurassic period (~150 million years ago). The other orders shown also contain non-eusocial species, including many lineages where eusociality was inferred to be the ancestral state. Thus the number of independent evolutions of eusociality is still under investigation. The major eusocial groups are shown in boldface in the phylogenetic tree.

Paradox

Prior to the gene-centered view of evolution, eusociality was seen as an apparent evolutionary paradox: if adaptive evolution unfolds by differential reproduction of individual organisms, how can individuals incapable of passing on their genes evolve and persist? In On the Origin of Species, Darwin referred to the existence of sterile castes as the "one special difficulty, which at first appeared to me insuperable, and actually fatal to my theory". Darwin anticipated that a possible resolution to the paradox might lie in the close family relationship, which W.D. Hamilton quantified a century later with his 1964 inclusive fitness theory. After the gene-centered view of evolution was developed in the mid 1970s, non-reproductive individuals were seen as an extended phenotype of the genes, which are the primary beneficiaries of natural selection.

Inclusive fitness and haplodiploidy

Further information: haplodiploidy

According to inclusive fitness theory, organisms can gain fitness not just through increasing their own reproductive output, but also via increasing the reproductive output of other individuals that share their genes, especially their close relatives. Individuals are selected to help their relatives when the cost of helping is less than the benefit gained by their relative multiplied by the fraction of genes that they share, i.e. when Cost < relatedness * Benefit. Under inclusive fitness theory, the necessary conditions for eusociality to evolve are more easily fulfilled by haplodiploid species because of their unusual relatedness structure.

In haplodiploid species, females develop from fertilized eggs and males develop from unfertilized eggs. Because a male is haploid, his daughters share 100% of his genes and 50% of their mother's. Therefore, they share 75% of their genes with each other. This mechanism of sex determination gives rise to what W. D. Hamilton first termed "supersisters" which are more related to their sisters than they would be to their own offspring. Even though workers often do not reproduce, they can potentially pass on more of their genes by helping to raise their sisters than they would by having their own offspring (each of which would only have 50% of their genes). This unusual situation, where females may have greater fitness when they help rear siblings rather than producing offspring, is often invoked to explain the multiple independent evolutions of eusociality (arising at least nine separate times) within the haplodiploid group Hymenoptera. While females share 75% of genes with their sisters in haplodiploid populations, they only share 25% of their genes with their brothers. Accordingly, the average relatedness of an individual to their sibling is 50%. Therefore, helping behavior is only advantageous if it is biased to helping sisters, which would drive the population to a 1:3 sex ratio of males to females. At this ratio, males, as the rarer sex, increase in reproductive value, negating the benefit of female-biased investment. 

However, not all eusocial species are haplodiploid (termites, some snapping shrimps, and mole rats are not). Conversely, many bees are haplodiploid yet are not eusocial, and among eusocial species many queens mate with multiple males, resulting in a hive of half-sisters that share only 25% of their genes. The association between haplodiploidy and eusociality is below statistical significance. Haplodiploidy alone is thus neither necessary nor sufficient for eusociality to emerge. However relatedness does still play a part, as monogamy (queens mating singly) has been shown to be the ancestral state for all eusocial species so far investigated.  If kin selection is an important force driving the evolution of eusociality, monogamy should be the ancestral state, because it maximizes the relatedness of colony members. 

Ecology

Many scientists citing the close phylogenetic relationships between eusocial and non-eusocial species are making the case that environmental factors are especially important in the evolution of eusociality. The relevant factors primarily involve the distribution of food and predators.

Increased parasitism and predation rates are the primary ecological drivers of social organization. Group living affords colony members defense against enemies, specifically predators, parasites, and competitors, and allows them to gain advantage from superior foraging methods.

With the exception of some aphids and thrips, all eusocial species live in a communal nest which provides both shelter and access to food resources. Mole rats, many bees, most termites, and most ants live in burrows in the soil; wasps, some bees, some ants, and some termites build above-ground nests or inhabit above-ground cavities; thrips and aphids inhabit galls (neoplastic outgrowths) induced on plants; ambrosia beetles and some termites nest together in dead wood; and snapping shrimp inhabit crevices in marine sponges. For many species the habitat outside the nest is often extremely arid or barren, creating such a high cost to dispersal that the chance to take over the colony following parental death is greater than the chance of dispersing to form a new colony. Defense of such fortresses from both predators and competitors often favors the evolution of non-reproductive soldier castes, while the high costs of nest construction and expansion favor non-reproductive worker castes.

The importance of ecology is supported by evidence such as experimentally induced reproductive division of labor, for example when normally solitary queens are forced together. Conversely, female Damaraland mole-rats undergo hormonal changes that promote dispersal after periods of high rainfall, supporting the plasticity of eusocial traits in response to environmental cues.

Climate also appears to be a selective agent driving social complexity; across bee lineages and Hymenoptera in general, higher forms of sociality are more likely to occur in tropical than temperate environments. Similarly, social transitions within halictid bees, where eusociality has been gained and lost multiple times, are correlated with periods of climatic warming. Social behavior in facultative social bees is often reliably predicted by ecological conditions, and switches in behavioral type have been experimentally induced by translocating offspring of solitary or social populations to warm and cool climates. In H. rubicundus, females produce a single brood in cooler regions and two or more broods in warmer regions, so the former populations are solitary while the latter are social. In another species of sweat bees, L. calceatum, social phenotype has been predicted by altitude and micro-habitat composition, with social nests found in warmer, sunnier sites, and solitary nests found in adjacent, cooler, shaded locations. Facultatively social bee species, however, which comprise the majority of social bee diversity, have their lowest diversity in the tropics, being largely limited to temperate regions.

Multilevel selection

Further information: Group selection

Once pre-adaptations such as group formation, nest building, high cost of dispersal, and morphological variation are present, between-group competition has been cited as a quintessential force in the transition to advanced eusociality. Because the hallmarks of eusociality will produce an extremely altruistic society, such groups will out-reproduce their less cooperative competitors, eventually eliminating all non-eusocial groups from a species. Multilevel selection has however been heavily criticized by some for its conflict with the kin selection theory.

Reversal to solitarity

A reversal to solitarity is an evolutionary phenomenon in which descendants of a eusocial group evolve solitary behavior once again. Bees have been model organisms for the study of reversal to solitarity, because of the diversity of their social systems. Each of the four origins of eusociality in bees was followed by at least one reversal to solitarity, giving a total of at least nine reversals. In a few species, solitary and eusocial colonies appear simultaneously in the same population, and different populations of the same species may be fully solitary or eusocial. This suggests that eusociality is costly to maintain, and can only persist when ecological variables favor it. Disadvantages of eusociality include the cost of investing in non-reproductive offspring, and an increased risk of disease.

All reversals to solitarity have occurred among primitively eusocial groups; none have followed the emergence of advanced eusociality. The "point of no return" hypothesis posits that the morphological differentiation of reproductive and non-reproductive castes prevents highly eusocial species such as the honeybee from reverting to the solitary state.

Physiological and developmental mechanisms

An understanding of the physiological causes and consequences of the eusocial condition has been somewhat slow; nonetheless, major advancements have been made in learning more about the mechanistic and developmental processes that lead to eusociality.

Involvement of pheromones

Pheromones are thought to play an important role in the physiological mechanisms underlying the development and maintenance of eusociality. In fact the evolution of enzymes involved both in the production and perception of pheromones has been shown to be important for the emergence of eusociality both within termites and in Hymenoptera. The most well-studied queen pheromone system in social insects is that of the honey bee Apis mellifera. Queen mandibular glands were found to produce a mixture of five compounds, three aliphatic and two aromatic, which have been found to control workers. Mandibular gland extracts inhibit workers from constructing queen cells in which new queens are reared which can delay the hormonally based behavioral development of workers and can suppress ovarian development in workers. Both behavioral effects mediated by the nervous system often leading to recognition of queens (releaser) and physiological effects on the reproductive and endocrine system (primer) are attributed to the same pheromones. These pheromones volatilize or are deactivated within thirty minutes, allowing workers to respond rapidly to the loss of their queen.

The levels of two of the aliphatic compounds increase rapidly in virgin queens within the first week after eclosion (emergence from the pupal case), which is consistent with their roles as sex attractants during the mating flight. It is only after a queen is mated and begins laying eggs, however, that the full blend of compounds is made. The physiological factors regulating reproductive development and pheromone production are unknown.

In several ant species, reproductive activity has also been associated with pheromone production by queens. In general, mated egg laying queens are attractive to workers whereas young winged virgin queens, which are not yet mated, elicit little or no response. However, very little is known about when pheromone production begins during the initiation of reproductive activity or about the physiological factors regulating either reproductive development or queen pheromone production in ants.

Among ants, the queen pheromone system of the fire ant Solenopsis invicta is particularly well studied. Both releaser and primer pheromones have been demonstrated in this species. A queen recognition (releaser) hormone is stored in the poison sac along with three other compounds. These compounds were reported to elicit a behavioral response from workers. Several primer effects have also been demonstrated. Pheromones initiate reproductive development in new winged females, called female sexuals. These chemicals also inhibit workers from rearing male and female sexuals, suppress egg production in other queens of multiple queen colonies and cause workers to execute excess queens. The action of these pheromones together maintains the eusocial phenotype which includes one queen supported by sterile workers and sexually active males (drones). In queenless colonies that lack such pheromones, winged females will quickly shed their wings, develop ovaries and lay eggs. These virgin replacement queens assume the role of the queen and even start to produce queen pheromones. There is also evidence that queen weaver ants Oecophylla longinoda have a variety of exocrine glands that produce pheromones, which prevent workers from laying reproductive eggs.

Similar mechanisms are used for the eusocial wasp species Vespula vulgaris. In order for a Vespula vulgaris queen to dominate all the workers, usually numbering more than 3000 in a colony, she exerts pheromone to signal her dominance. The workers were discovered to regularly lick the queen while feeding her, and the air-borne pheromone from the queen's body alerts those workers of her dominance.

The mode of action of inhibitory pheromones which prevent the development of eggs in workers has been convincingly demonstrated in the bumble bee Bombus terrestris. In this species, pheromones suppress activity of the corpora allata and juvenile hormone (JH) secretion. The corpora allata is an endocrine gland that produces JH, a group of hormones that regulate many aspects of insect physiology. With low JH, eggs do not mature. Similar inhibitory effects of lowering JH were seen in halictine bees and polistine wasps, but not in honey bees.

Other strategies

A variety of strategies in addition to the use of pheromones have evolved that give the queens of different species of social insects a measure of reproductive control over their nest mates. In many Polistes wasp colonies, monogamy is established soon after colony formation by physical dominance interactions among foundresses of the colony including biting, chasing, and food soliciting. Such interactions created a dominance hierarchy headed by individuals with the greatest ovarian development. Larger, older individuals often have an advantage during the establishment of dominance hierarchies. The rank of subordinates is positively correlated with the degree of ovarian development and the highest ranking individual usually becomes queen if the established queen disappears. Workers do not oviposit when queens are present because of a variety of reasons: colonies tend to be small enough that queens can effectively dominate workers, queens practice selective oophagy or egg eating, or the flow of nutrients favors queen over workers and queens rapidly lay eggs in new or vacated cells. However, it is also possible that morphological differences favor the worker. In certain species of wasps, such as Apoica flavissima queens are smaller than their worker counterparts. This can lead to interesting worker-queen dynamics, often with the worker policing queen behaviors. Other wasps, like Polistes instabilis have workers with the potential to develop into reproductives, but only in cases where there are no queens to suppress them.

In primitively eusocial bees (where castes are morphologically similar and colonies usually small and short-lived), queens frequently nudge their nest mates and then burrow back down into the nest. This behavior draws workers into the lower part of the nest where they may respond to stimuli for cell construction and maintenance. Being nudged by the queen may play a role in inhibiting ovarian development and this form of queen control is supplemented by oophagy of worker laid eggs. Furthermore, temporally discrete production of workers and gynes (actual or potential queens) can cause size dimorphisms between different castes as size is strongly influenced by the season during which the individual is reared. In many wasp species worker caste determination is characterized by a temporal pattern in which workers precede non-workers of the same generation. In some cases, for example in the bumble bee, queen control weakens late in the season and the ovaries of workers develop to an increasing extent. The queen attempts to maintain her dominance by aggressive behavior and by eating worker laid eggs; her aggression is often directed towards the worker with the greatest ovarian development.

In highly eusocial wasps (where castes are morphologically dissimilar), both the quantity and quality of food seem to be important for caste differentiation. Recent studies in wasps suggest that differential larval nourishment may be the environmental trigger for larval divergence into one of two developmental classes destined to become either a worker or a gyne. All honey bee larvae are initially fed with royal jelly, which is secreted by workers, but normally they are switched over to a diet of pollen and honey as they mature; if their diet is exclusively royal jelly, however, they grow larger than normal and differentiate into queens. This jelly seems to contain a specific protein, designated as royalactin, which increases body size, promotes ovary development, and shortens the developmental time period. Furthermore, the differential expression in Polistes of larval genes and proteins (also differentially expressed during queen versus caste development in honey bees) indicate that regulatory mechanisms may occur very early in development.