Gene-centered view of evolution

The gene-centered view of evolution, gene selection theory or selfish gene theory holds that natural selection acts through differential survival of competing genes, increasing the frequency of those alleles whose phenotypic effects successfully promote their own propagation. According to this theory, adaptations are the phenotypic effects through which genes achieve their propagation.

Evolution by natural selection
The scientific explanation for the adaptation of living beings was initially tailored by Charles Darwin and Alfred Russel Wallace, who proposed the theory of evolution by natural selection (Darwin & Wallace, 1858). According to this theory, a population of reproductive individuals is subject to natural selection if the following are present: (1) variation in the reproductive performance of individuals within the population; (2) heredity, meaning "like begets like"; and (3) competition for the resources required for reproduction, be it fertile mates or food. So, those characteristics that augment reproductive performance tend to be represented at a greater proportion than their competing alternative.

The theory of evolution by natural selection was initially based on a vague concept of heredity. Darwin endorsed the blending inheritance hypothesis due to the absence, at that time, of a rigorous theory of heredity. Subsequently, significant discoveries about both the mechanisms of inheritance and those of development have revolutionised this area of biology.

Discoveries in heredity
In the mid-19th century, the Czech Augustinian monk Gregor Mendel proposed the particulate inheritance theory, which states that genes are preserved during development and are passed on unchanged (Fisher, 1930). According to this theory, genes can and usually do mix their phenotypic effects in an organism, but themselves are not mixed and are transmitted in an "all-or-nothing" mode to the next generation.

The biologist August Weismann proposed the continuity of the germ plasm, where phenotypic changes environmentally caused in the soma are not converted into changes in the genotype (Weismann, 1893). The classic illustration of this principle is that even if you cut off the tails of thousands of generations of rats, they will always produce tailed offspring.

This principle was reflected at molecular level by Francis Crick when he formulated the central dogma of molecular biology in 1958: information flows only from nucleic acid to nucleic acid or protein, and never from protein to nucleic acid or protein.

These discoveries made it clear that the inheritance of acquired characters was not an evolutionary factor and identified genes as lasting entities that survive through many generations. Maynard Smith summarized the issue:

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, 1998, p.10)

The rejection of the inheritance of acquired characters combined with the classical mathematical evolutionary biology developed by Ronald Fisher (particularly in his 1930 book, The Genetical Theory of Natural Selection), J. B. S. Haldane and Sewall Wright, they paved the way to the formulation of the selfish gene theory.

The gene as the unit of selection
The view of the gene as the unit of selection was developed mainly in the books Adaptation and Natural Selection, by George C. Williams, and in The Selfish Gene and The Extended Phenotype, both by Richard Dawkins. It had earlier been proposed by Colin Pittendrigh in his 1958 article, Adaptation, natural selection, and behavior, and in the classic papers about altruism of 1963 and 1964 by William Hamilton.

According to Williams' 1966 book:

The 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, p.22-23)

Williams argued that "The natural selection of phenotypes cannot in itself produce cumulative change, because phenotypes are extremely temporary manifestations." (Williams, 1966) Each phenotype is the unique product of the interaction between genome and environment. It doesn't 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 sequence of DNA can have a high permanence and a low rate of endogenous change. The question that remains is how long the segment must be.

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." (Williams, 1966) Only half of it is transmitted to each descendant due to the independent segregation, and only fragments of it are transmitted because of recombination.

If the gene is defined as "that which segregates and recombines with appreciable frequency", it will generally fulfill the requisite of high degree of permanence and a low rate of endogenous change. The gene as an informational entity persists for an evolutionary 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 further expound 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 reverse-engineers the purpose in the mind of the Divine Engineer of Nature, or the Utility Function of God. In the end, Dawkins shows that it is a mistake to assume that an ecosystem or a species as a whole exists for a purpose. In fact, it is wrong 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.

Genic selection
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 difference in these phenotypic differences. 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." (Williams, 1985) In other words, we expect selfish genes, "selfish" meaning that promotes its own survival without necessarily promoting the survival of the organism, group or even species. This theory implicates that adaptations are the phenotypic effects of genes to maximize their representation in the future generations. An adaptation is maintained by selection if it promotes genetic survival directly or some subordinate goal that ultimately contributes to successful reproduction.

Vehicles
As stated above, genes are not naked in the world. They 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" (Haig, 1997). They build vehicles to promote their mutual interests of jumping into the next generation of vehicles. As Dawkins put 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 may be enough to enable 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" (Cronin, 1991). 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.

Individual altruism, 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 doesn't matter from the gene's point of view. (Williams, 1992) A selfish gene could be favoured 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 forego 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 have 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.

Green-beard effects gained their name from a thought-experiment of Richard Dawkins (1976), 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, a '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.

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 was 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 cheats during meiosis or gametogenesis and ends up in more than half of the functional gametes. These genes persist even resulting in reduced fertility. Egbert Leigh (1971) 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.

Challenges to the "Selfish Gene"
Those prominent among the opponents of this gene-centric view of evolution include paleontologist Stephen Jay Gould (September 10, 1941 – May 20, 2002) and philosopher Elliot Sober, who have disputed the theory's applicability and fruitfulness. Gould has characterized this perspective as confusing book-keeping with causality. Gould views selection working on many levels, and has called attention for a hierarchical perspective of selection. Gould has also called the position "strict adaptationism," "ultra-Darwinism," and "Darwinian fundamentalism," describing it as "reductionist." He saw it as leading to a simplistic "algorithmic" theory of evolution, or even to the re-introduction of a teleological principle.

Such challenges may be phenomenological in character, derived, in part, from common-sense analysis of the "experience" of evolution. Interestingly, Dawkins has further extended the selfish gene concept to psycho-sociology with the notion of "memes"--which might be described as a bid to make sociology as "fundamental" a science as particle physics or genetics.

Summary
The selfish gene theory 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 genes whose phenotypic effects successfully promote their own propagation will be favourably selected in detriment to their competitors. This process produces adaptations to the benefit of genes, which promotes the reproductive success of the organism, or of others organisms containing the same gene (kin altruism and green-beard effects), or even only its own propagation in detriment to the other genes of the genome (intragenomic conflict).

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