Gene-centric view of evolution

The gene-centric 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.

Improbable Functional Organization
The fundamental characteristic of all biological systems, in contrast to those non-biologicals, is their improbable functional organization. Organisms are composed of different parts organized in such a way that their interaction produce a highly improbable functional result. This organization is amazing because the appropriateness of the means to the end transmits a powerful illusion of intentional design (Williams, 1966). In fact, William Paley stated that the perfection of living beings, exemplified by the human eye, could only come about through the action of a creator with superior intelligence (Dawkins, 1986).

The problem comes down to the improbability of finding, in the giant mathematical space of all possible arrangements of matter, that tiny minority of functional arrangements capable of performing those feats accomplished by actual living beings (Dawkins, 1986). The astronomer Fred Hoyle illustrated this argument stating that the likelihood of a functional molecule like hemoglobin emerge by chance is similar to that of a "a tornado sweeping through a junk-yard might assemble a Boeing 747 from the materials therein."

Evolution by Natural Selection
The scientific explanation to this mistery began to be tailored by Charles Darwin and Alfred Russell 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 presents: (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 females or food. So, those characters that augments reproductive performance tend to be represented at a greater proportion than its competing alternatives.

The theory of evolution by natural selection was initially based on a vague concept of heredity. Even Darwin endorsed the blending inheritance hypothesis due to the lack on an appropriate theory of heredity. But, new discoveries about the mechanisms of inheritance and development were made in the following decades and clarified the issue.

Discoveries in Heredity
The 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 enviromentally 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 the tail 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: informations flows only from nucleic acid to nucleic acid or protein, and never from protein to nucleic acid or protein.

This discoveries completely ruled out the inheritance of acquired characters as an evolutionary factor, and also identified genes as the lasting entities that survives through many generations. In conjunction to the 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 mainly developed in the books Adaptation and Natural Selection, by George C. Williams, and also in The Selfish Gene and The Extended Phenotype, both by Richard Dawkins. Even though, it was already present in the article of 1958 Adaptation, natural selection, and behavior by Colin Pittendrigh, 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 certains 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)"

So, "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 is known that DNA is the 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?"

An entire sexual genome is the unique combination of father's and mother's chromosomes produced at the moment of fertilization. It will be 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.

The gene, defined as "that which segregates and recombines with appreciable frequency", is the only entity that fulfills 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.

Genic Selection
The 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 to survive and neutral or altruistic genes to be eliminated. 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 promotes genetic survival directly or some subordinate goal that ultimately contributes to successful reproduction.

Vehicles
As said above, genes are not naked in the world. They usually are packed together inside a genome, which itself is 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, we are the "survival machines" of genes.

The phenotypic effect of a particular gene is contingent to its environment, including the other fellow genes that constitutes with it the total genome. A gene almost never have a fixed effect, so how is possible to speak of gene for long legs? It is due to the fact that you can talk about phenotypic differences between alleles. One can say that one allele, everything alse constant or varying among certains limits, causes greater legs than its alternative. This difference is enough to the allow 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 succes at a young age, but also cause a greater likelihood of death at a later age. If the benefit is greater than the harm, the gene shall be positively selected.

Individual Altruism, Genetic Egoism
The gene is an unit of hereditary information that exist 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 can 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 forgoes 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 pedicts that a gene may recognize 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, everything else constant, greater altruism among brothers than among cousins.

Green-beard effects gained their name from a thought-experiment of 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 directs 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 promote 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.

Summary
The selfish gene theory is the synthesis between 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 promotes successfully their own propagation will be favorably 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 of 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.