Unit of selection

A unit of selection is a biological entity within the hierarchy of biological organisation (e.g. genes, cells, individuals, groups, species) that is subject to natural selection. For several decades there has been intense debate among evolutionary biologists about the extent to which evolution has been shaped by selective pressures acting at these different levels. This debate has been as much about what it means to be a unit of selection as it has about the relative importance of the units themselves, i.e., is it group or individual selection that has driven the evolution of altruism? When it is noted that altruism reduces the fitness of individuals, it is difficult to see how altruism has evolved within the context of Darwinian selection acting on individuals; see Kin selection.

Examples of selection at each level
Below, cases of selection at the genic, cellular, individual and group level from within the multi-level selection perspective are presented and discussed.

Selection at the level of the gene

 * Main article: gene-centered view of evolution

George C. Williams in his influential book Adaptation and Natural Selection was one of the first to present a gene-centered view of evolution with the gene as the unit of selection, arguing that a unit of selection should exhibit a high degree of permanence.

Richard Dawkins has written several books popularizing and expanding the idea. According to Dawkins, genes cause phenotypes and a gene is 'judged' by its phenotypic effects. Dawkins distinguishes entities which survive or fail to survive ("replicators") from entities with temporary existence that interact directly with the environment ("vehicles"). Genes are "replicators" whereas individuals and groups of individuals are "vehicles". Dawkins argues that, although they are both aspects of the same process, "replicators" rather than "vehicles" should be preferred as units of selection. This is because replicators, owing to their permanence, should be regarded as the ultimate beneficiaries of adaptations. Genes are replicators and therefore the gene is the unit of selection.

Critics of Dawkins, such as philosopher of biology Elliot Sober, have rejected the gene as a universal unit of selection by emphasizing the causal mechanisms of selection. A unit of selection, according to Sober, is an entity whose properties cause differential reproduction. In this case the causes of one and the same selection process could, in some instances, be correctly described at different levels in the biological hierarchy. However, according to Sober, this does not generally apply at the genic level. Sober argues that a gene's phenotypic effects can depend on context. If a gene increases reproductive success in one context but lowers it in another it has no such thing as an overall causal role.

Some clear-cut examples of selection at the level of the gene include meiotic drive and retrotransposons. In both of these cases, gene sequences increase their relative frequency in a population without necessarily providing benefits at other levels of organization. Meiotic-drive mutations (see segregation distortion) manipulate the machinery of chromosomal segregation so that chromosomes carrying the mutation are later found in more than half of the gametes produced by individuals heterozygous for the mutation, and for this reason the frequency of the mutation increases in the population. Retrotransposons are DNA sequences that generate copies of themselves that later insert themselves in the genome more or less randomly. Such insertions can be very mutagenic and thus reduce drastically individual fitness, so that there is strong selection against elements that are very active. Meiotic-drive alleles have also been shown strongly to reduce individual fitness, clearly exemplifying the potential conflict between selection at different levels.

Selection at the level of the cell
Leo Buss in his book The Evolution of Individuality proposes that much of the evolution of development in metazoans reflects the conflict between selective pressures acting at the level of the cell and those acting at the level of the multicellular individual. This perspective allows one to make sense straightforwardly of phenomena as diverse as cancer, gastrulation, and germ line sequestration. Cancer, e.g., occurs when individual cells in the body mutate and develop the ability of proliferating without the restrains acting on normal cells which this way are forced to serve the needs of the individual organism. However, one must be careful not to abuse such verbalizations to avoid trivializing them. The proliferation of specific cells of the vertebrate immune system to fight off infecting pathogens, e.g., could be described as a case of cellular selection, but it is better described as a case of programmed and exquisitely contained cellular proliferation.

Selection at the level of individual organism
Selection at the level of the organism can be described as Darwinism, and is well understood and considered common. If a relatively faster gazelle manages to survive and reproduce more, the causation of the higher fitness of this gazelle can be fully accounted for if one looks at how individual gazelles fare under predation. The speed of the faster gazelle could be caused by a single gene, be polygenic, or be fully environmentally determined, but the unit of selection in this case is the individual since speed is a property of each individual gazelle. In The Selfish Gene, Dawkins refers to this as a survival machine.

Selection at the level of the group

 * Main article: Group selection

If a group of organisms, owing to their interactions or division of labor, provides superior fitness compared to other groups, where the fitness of the group is higher or lower than the mean fitness of the constituent individuals, group selection can be declared to occur..

Specific syndromes of selective factors can create situations in which groups are selected because they display group properties which are selected-for. Some mosquito-transmitted rabbit viruses, for instance, are only transmitted to uninfected rabbits from infected rabbits which are still alive. This creates a selective pressure on every group of viruses already infecting a rabbit not to become too virulent and kill their host rabbit before enough mosquitoes have bitten it, since otherwise all the viruses inside the dead rabbit would rot with it. And indeed in natural systems such viruses display much lower virulence levels than do mutants of the same viruses that in laboratory culture readily outcompete non-virulent variants (or than do tick-transmitted viruses since ticks do bite dead rabbits).

Species selection and selection at higher taxonomic levels
It remains controversial among biologists whether selection can operate at and above the level of species. One particular defender of the idea of species selection was S.J. Gould who proposed the view that there exist macroevolutionary processes which shape evolution at and above the level of species and are not driven by the microevolutionary mechanisms that are the basis of the Modern Synthesis. If one views species as individuals that replicate (speciate) and die (go extinct), then species could be subject to selection and thus could change their occurrence over geological time, much as heritable selected-for traits change theirs over the generations.

For evolution to be driven by species selection, differential success must be the result of selection upon species-intrinsic properties, rather than for properties of genes, cells, individuals, or populations within species. Such properties include, for example, population structure, their propensity to speciate, extinction rates, and geological persistence. While the fossil record shows differential persistence of species, examples of species-intrinsic properties subject to natural selection have been much harder to document.