Unit of selection
Encyclopedia
A unit of selection is a biological entity within the hierarchy of biological organisation (e.g. self-reproducing molecules
genes
, cell
s, 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, e.g., is it group or individual selection that has driven the evolution of altruism
? When it is noted that altruism reduces the fitness of individuals, gene- or individual-centered explanations for the evolution of altruism become more complex and rely on the use of game theory, for instance; see Kin selection
and group selection
.
classic piece "The Units of Selection" and John Maynard-Smith and Eörs Szathmáry
's co-authored book, The Major Transitions in Evolution
. As a theoretical introduction to what is at stake vis-a-vis units of selection, Lewontin writes:
Elisabeth Lloyd
's book The Structure and Confirmation of Evolutionary Theory provides a basic philosophical introduction to the debate.
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. Dawkins further expounded this view in an entire chapter called 'God's utility function
' in the book River Out of Eden
where he explained that only genes alone have utility functions.
Some clear-cut examples of selection at the level of the gene include meiotic drive and retrotransposon
s. 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.
Retrotransposon
s 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.
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 can shed new light on 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 to proliferate without the restraints normally in place that serve the interests of the individual organism.
This selection for unconstrained proliferation is in conflict with the fitness interests of the individual, and thus there is tension between selection at the level of the cell and selection at the level of the individual. Since the proliferation of specific cells of the vertebrate immune system to fight off infecting pathogens is a case of programmed and exquisitely contained cellular proliferation, it represents a case of the individual manipulating selection at the level of the cell to enhance its own fitness. In the case of the vertebrate immune system, selection at the level of the cell and individual are not in conflict.
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'.
Specific syndromes of selective factors can create situations in which groups are selected because they display group properties which are selected-for. Many common examples of group traits are reducible to individual traits, however. Selection of these traits is thus more simply explained as selection of individual traits.
"Some mosquito-transmitted rabbit viruses 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)."
In the previous passage, the group is assumed to have "lower virulence", i.e., "virulence" is presented as a group trait. One could argue then that the selection is in fact against individual viruses that are too virulent. In this case, however, the fitness of all viruses within a rabbit is affected by what the group does to the rabbit. Indeed the proper, directly selected group property is that of "not killing the rabbit too early" rather than individual virulence. In situations such as these, we would expect there to be selection for cooperation amongst the viruses in a group in such a way that the group will not "kill the rabbit too early". It is of course true that any group behavior is the result of individual traits, such as individual viruses suppressing the virulence of their neighbours, but the causes of phenotypes are rarely the causes of fitness differences.
who proposed the view that there exist macroevolution
ary processes which shape evolution that are not driven by the microevolution
ary mechanisms that are the basis of the Modern Synthesis
. If one views species as entities 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 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.
RNA world hypothesis
The RNA world hypothesis proposes that life based on ribonucleic acid pre-dates the current world of life based on deoxyribonucleic acid , RNA and proteins. RNA is able both to store genetic information, like DNA, and to catalyze chemical reactions, like an enzyme protein...
genes
Gênes
Gênes is the name of a département of the First French Empire in present Italy, named after the city of Genoa. It was formed in 1805, when Napoleon Bonaparte occupied the Republic of Genoa. Its capital was Genoa, and it was divided in the arrondissements of Genoa, Bobbio, Novi Ligure, Tortona and...
, cell
Cell (biology)
The cell is the basic structural and functional unit of all known living organisms. It is the smallest unit of life that is classified as a living thing, and is often called the building block of life. The Alberts text discusses how the "cellular building blocks" move to shape developing embryos....
s, individuals, groups
Deme
In Ancient Greece, a deme or demos was a subdivision of Attica, the region of Greece surrounding Athens. Demes as simple subdivisions of land in the countryside seem to have existed in the 6th century BC and earlier, but did not acquire particular significance until the reforms of Cleisthenes in...
, species
Species
In biology, a species is one of the basic units of biological classification and a taxonomic rank. A species is often defined as a group of organisms capable of interbreeding and producing fertile offspring. While in many cases this definition is adequate, more precise or differing measures are...
) that is subject to natural selection
Natural selection
Natural selection is the nonrandom process by which biologic traits become either more or less common in a population as a function of differential reproduction of their bearers. It is a key mechanism of evolution....
. 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, e.g., is it group or individual selection that has driven the evolution of altruism
Altruism
Altruism is a concern for the welfare of others. It is a traditional virtue in many cultures, and a core aspect of various religious traditions, though the concept of 'others' toward whom concern should be directed can vary among cultures and religions. Altruism is the opposite of...
? When it is noted that altruism reduces the fitness of individuals, gene- or individual-centered explanations for the evolution of altruism become more complex and rely on the use of game theory, for instance; see Kin selection
Kin selection
Kin selection refers to apparent strategies in evolution that favor the reproductive success of an organism's relatives, even at a cost to the organism's own survival and reproduction. Charles Darwin was the first to discuss the concept of group/kin selection...
and group selection
Group selection
In evolutionary biology, group selection refers to the idea that alleles can become fixed or spread in a population because of the benefits they bestow on groups, regardless of the alleles' effect on the fitness of individuals within that group....
.
Fundamental theory
Two useful introductions to the fundamental theory underlying the unit of selection issue and debate, which also present examples of multi-level selection from the entire range of the biological hierarchy (typically with entities at level N-1 competing for increased representation, i.e., higher frequency, at the immediately higher level N, e.g., organisms in populations or cell lineages in organisms), are Richard Lewontin'sRichard Lewontin
Richard Charles "Dick" Lewontin is an American evolutionary biologist, geneticist and social commentator. A leader in developing the mathematical basis of population genetics and evolutionary theory, he pioneered the notion of using techniques from molecular biology such as gel electrophoresis to...
classic piece "The Units of Selection" and John Maynard-Smith and Eörs Szathmáry
Eörs Szathmáry
Eörs Szathmáry is a Hungarian theoretical evolutionary biologist at the late Collegium Budapest Eörs Szathmáry (born 1959) is a Hungarian theoretical evolutionary biologist at the late Collegium Budapest Eörs Szathmáry (born 1959) is a Hungarian theoretical evolutionary biologist at the late...
's co-authored book, The Major Transitions in Evolution
The Major Transitions in Evolution
The Major Transitions in Evolution is a book written by John Maynard Smith and Eörs Szathmáry . This was a seminal publication that continues to contribute to ongoing issues in evolutionary biology....
. As a theoretical introduction to what is at stake vis-a-vis units of selection, Lewontin writes:
The generality of the principles of natural selection means that any entities in nature that have variation, reproduction, and heritability may evolve. ...the principles can be applied equally to genes, organisms, populations, species, and at opposite ends of the scale, prebiotic molecules and ecosystems." (1970, pp. 1-2)
Elisabeth Lloyd
Elisabeth Lloyd
Elisabeth Anne Lloyd is a philosopher of biology. She currently holds the Arnold and Maxine Tanis Chair of History and Philosophy of Science and is also Professor of Biology, Adjunct Professor of Philosophy at Indiana University, Affiliated Faculty Scholar at the Kinsey Institute for Research in...
's book The Structure and Confirmation of Evolutionary Theory provides a basic philosophical introduction to the debate.
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
George C. WilliamsGeorge C. Williams
Professor George Christopher Williams was an American evolutionary biologist.Williams was a professor emeritus of biology at the State University of New York at Stony Brook. He was best known for his vigorous critique of group selection. The work of Williams in this area, along with W. D...
in his influential book Adaptation and Natural Selection
Adaptation and Natural Selection
Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought is a 1966 book by the American evolutionary biologist George C. Williams...
was one of the first to present a gene-centered view of evolution
Gene-centered view of evolution
The gene-centered view of evolution, gene selection theory or selfish gene theory holds that evolution occurs through the differential survival of competing genes, increasing the frequency of those alleles whose phenotypic effects successfully promote their own propagation, with gene defined as...
with the gene as the unit of selection, arguing that a unit of selection should exhibit a high degree of permanence.
Richard Dawkins
Richard Dawkins
Clinton Richard Dawkins, FRS, FRSL , known as Richard Dawkins, is a British ethologist, evolutionary biologist and author...
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. Dawkins further expounded this view in an entire chapter called 'God's utility function
God's utility function
God's utility function is a phrase coined by Richard Dawkins in his book River Out of Eden. "God's utility function" is the third chapter in this book. Dawkins uses this phrase to expound the Gene-centered view of evolution by equating the phrase to the meaning of life or the purpose of life...
' in the book River Out of Eden
River out of Eden
River Out of Eden: A Darwinian View of Life is a 1995 popular science book by Richard Dawkins. The book is about Darwinian evolution and includes summaries of the topics covered in his earlier books, The Selfish Gene, The Extended Phenotype and The Blind Watchmaker. It is part of the Science...
where he explained that only genes alone have utility functions.
Some clear-cut examples of selection at the level of the gene include meiotic drive and retrotransposon
Retrotransposon
Retrotransposons are genetic elements that can amplify themselves in a genome and are ubiquitous components of the DNA of many eukaryotic organisms. They are a subclass of transposon. They are particularly abundant in plants, where they are often a principal component of nuclear DNA...
s. 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.
Retrotransposon
Retrotransposon
Retrotransposons are genetic elements that can amplify themselves in a genome and are ubiquitous components of the DNA of many eukaryotic organisms. They are a subclass of transposon. They are particularly abundant in plants, where they are often a principal component of nuclear DNA...
s 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 BussLeo Buss
Leo W. Buss is a Professor in Yale University's departments of geology, geophysics, and ecology and evolutionary biology.-Life:He graduated from Johns Hopkins University with a B.A., M.A., and Ph.D in 1979....
in his book The Evolution of Individuality proposes that much of the evolution of development
Evolutionary developmental biology
Evolutionary developmental biology is a field of biology that compares the developmental processes of different organisms to determine the ancestral relationship between them, and to discover how developmental processes evolved...
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 can shed new light on phenomena as diverse as cancer
Cancer
Cancer , known medically as a malignant neoplasm, is a large group of different diseases, all involving unregulated cell growth. In cancer, cells divide and grow uncontrollably, forming malignant tumors, and invade nearby parts of the body. The cancer may also spread to more distant parts of the...
, gastrulation
Gastrulation
Gastrulation is a phase early in the embryonic development of most animals, during which the single-layered blastula is reorganized into a trilaminar structure known as the gastrula. These three germ layers are known as the ectoderm, mesoderm, and endoderm.Gastrulation takes place after cleavage...
, and germ line sequestration. Cancer, e.g., occurs when individual cells in the body mutate and develop the ability to proliferate without the restraints normally in place that serve the interests of the individual organism.
This selection for unconstrained proliferation is in conflict with the fitness interests of the individual, and thus there is tension between selection at the level of the cell and selection at the level of the individual. Since the proliferation of specific cells of the vertebrate immune system to fight off infecting pathogens is a case of programmed and exquisitely contained cellular proliferation, it represents a case of the individual manipulating selection at the level of the cell to enhance its own fitness. In the case of the vertebrate immune system, selection at the level of the cell and individual are not in conflict.
Selection at the level of individual organism
Selection at the level of the organism can be described as Darwinism
Darwinism
Darwinism is a set of movements and concepts related to ideas of transmutation of species or of evolution, including some ideas with no connection to the work of Charles Darwin....
, 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
The Selfish Gene
The Selfish Gene is a book on evolution by Richard Dawkins, published in 1976. It builds upon the principal theory of George C. Williams's first book Adaptation and Natural Selection. Dawkins coined the term "selfish gene" as a way of expressing the gene-centred view of evolution as opposed to the...
, Dawkins
Richard Dawkins
Clinton Richard Dawkins, FRS, FRSL , known as Richard Dawkins, is a British ethologist, evolutionary biologist and author...
refers to this as a 'survival machine'.
Selection at the level of the group
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. Many common examples of group traits are reducible to individual traits, however. Selection of these traits is thus more simply explained as selection of individual traits.
"Some mosquito-transmitted rabbit viruses 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)."
In the previous passage, the group is assumed to have "lower virulence", i.e., "virulence" is presented as a group trait. One could argue then that the selection is in fact against individual viruses that are too virulent. In this case, however, the fitness of all viruses within a rabbit is affected by what the group does to the rabbit. Indeed the proper, directly selected group property is that of "not killing the rabbit too early" rather than individual virulence. In situations such as these, we would expect there to be selection for cooperation amongst the viruses in a group in such a way that the group will not "kill the rabbit too early". It is of course true that any group behavior is the result of individual traits, such as individual viruses suppressing the virulence of their neighbours, but the causes of phenotypes are rarely the causes of fitness differences.
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 Stephen Jay GouldStephen Jay Gould
Stephen Jay Gould was an American paleontologist, evolutionary biologist, and historian of science. He was also one of the most influential and widely read writers of popular science of his generation....
who proposed the view that there exist macroevolution
Macroevolution
Macroevolution is evolution on a scale of separated gene pools. Macroevolutionary studies focus on change that occurs at or above the level of species, in contrast with microevolution, which refers to smaller evolutionary changes within a species or population.The process of speciation may fall...
ary processes which shape evolution that are not driven by the microevolution
Microevolution
Microevolution is the changes in allele frequencies that occur over time within a population. This change is due to four different processes: mutation, selection , gene flow, and genetic drift....
ary mechanisms that are the basis of the Modern Synthesis
Modern evolutionary synthesis
The modern evolutionary synthesis is a union of ideas from several biological specialties which provides a widely accepted account of evolution...
. If one views species as entities 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 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.
External links
- Dawkins, R.Richard DawkinsClinton Richard Dawkins, FRS, FRSL , known as Richard Dawkins, is a British ethologist, evolutionary biologist and author...
(1994). "Burying the Vehicle. Commentary on Wilson & Sober: Group Selection." Behavioural and Brain Sciences. 17 (4): 616-617 - Dusek, Val. (2002) "Lewontin’s Living Legacy: Levels of Selection and Organismic Construction of the Environment." Human Nature Review. 2: 367-374.
- Lloyd, Elisabeth, "Units and Levels of Selection." The Stanford Encyclopedia of Philosophy, (Fall 2005 Edition), Edward N. Zalta (ed.)
- Mayr, E.Ernst MayrErnst Walter Mayr was one of the 20th century's leading evolutionary biologists. He was also a renowned taxonomist, tropical explorer, ornithologist, historian of science, and naturalist...
(1997). "The objects of selection Proc. Natl. Acad. Sci. USA 94 (March): 2091-94. - Wilson, D.S. (2006). Human groups as adaptive units: toward a permanent consensus. In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition. Oxford: Oxford University Press. Full text