Supergene
Encyclopedia
A supergene is a group of neighbouring gene
s on a chromosome
which are inherited together because of close genetic linkage
and are functionally related in an evolutionary sense, although they are rarely co-regulated genetically.
Supergenes have cis-effect
s due to multiple loci
(which may be within a gene, or within a single gene's regulatory region), and tight linkage. They are classically polymorphic
, and different elements code for different fitness effects which combine to form a coherent or epistatic
whole. The two classic supergenes are (1) the Primula
heterostyly
locus, which controls "pin" and "thrum" types, and (2) the locus controlling Batesian mimetic
polymorphism in Papilio memnon
butterflies. For example, pin and thrum morphs of Primula have effects on genetic compatibility (pin style x thrum pollen
, or thrum style x pin pollen matings are successful, while pin x pin, and thrum x thrum matings are rarely successful due to pollen-style incompatibility
), and have different style length, anther height in the corolla tube, pollen size, and papilla size on the stigma. Each of these effects is controlled by a different locus in the same supergene, but recombinants are occasionally found with traits combining those of "pin" and "thrum" morphs.
Gene complexes, in contrast, are simply tightly linked groups of genes, often created via gene duplication
(sometimes called segmental duplication
if the duplicates remain side-by-side). Here, each gene has similar though slightly diverged function. For example, the human major histocompatibility complex (MHC)
region is a complex of tightly linked genes all acting in the immune system, but has no claim to be a supergene, even though the component genes very likely have epistatic effects and are in strong disequilibrium due in part to selection.
No supergene has yet been characterized to the functional DNA
level, but work is proceeding in a number of species.
The earliest use of the term "supergene" may be in an article by A. Ernst (1936) in the journal Archiv der Julzus Klaus-stiftung fur Vererbungsforschung, Sozialanthropologie und Rassenhygiene.
, due to selection for particular multilocus phenotype
s. For instance, in Batesian mimicry supergenes in species such as Papilio memnon, genes are required to affect hind-wing, fore-wing, and body colour, and also the presence or absence of long projections (the "tails" of swallowtail butterflies).
The case for the accumulative origin for supergenes was originally based on the work of Nabours on polymorphism
for colour and pattern in Grouse Locusts (Tetrigidae). In Acridium arenosum the colour-patterns are controlled by thirteen genes on the same chromosome, which reassort (recombine) fairly easily. They also occur in Apotettix eurycephalus where they form two tightly linked groups, between which there is 7% crossing-over. Furthermore, in Paratettix texanus there appears to be complete suppression of crossing-over among 24 out of 25 of the colour-pattern genes, which can be distinguished by comparing their effects with those found in other species. Analysis of Nabour's data by Darlington & Mather
concluded that the genes responsible for the morphs of Paratettix texanus have been gradually aggregated into a group which acts as a single switch-mechanism. This explanation was accepted by E.B. Ford
and incorporated into his accounts of ecological genetics.
This process might involve suppression of crossing-over, translocation of chromosome fragments and possibly occasional cistron duplication. That crossing-over can be suppressed by selection has been known for many years; Detlefsen and Roberts were able to reduce recombination between the loci for white eyes (w) and miniature wings (m) in Drosophila melanogaster from the normal 36% to 6% in one line and 0.6% in another.
Debate has tended to centre round the question, could the component genes in a super-gene have started off on separate chromosomes, with subsequent reorganization, or is it necessary for them to start on the same chromosome? Many scientists today believe the latter, because some linkage disequilibrium
is initially needed to select for tighter linkage, and linkage disequilibrium requires both the previous existence of polymorphisms via some other process, like natural selection, favouring gene combinations. If genes are weakly linked, it is probable that the rarer advantageous haplotype
dies out, leading to the loss of polymorphism at the other locus.
Most people, following J.R.G. Turner, therefore argue that supergenes arose in situ due to selection for correlated and epistatic traits, which just happened to have been possible to select via the existence of suitable loci closely linked to the original variant. Turner calls this a "sieve" explanation, and the Turner explanation might be called the "Turner sieve" hypothesis. Maynard Smith
agreed with this view in his authoritative textbook. Nevertheless, the question is not definitively settled. The problem is connected to an even larger question, the evolution of evolvability
.
Gene
A gene is a molecular unit of heredity of a living organism. It is a name given to some stretches of DNA and RNA that code for a type of protein or for an RNA chain that has a function in the organism. Living beings depend on genes, as they specify all proteins and functional RNA chains...
s on a chromosome
Chromosome
A chromosome is an organized structure of DNA and protein found in cells. It is a single piece of coiled DNA containing many genes, regulatory elements and other nucleotide sequences. Chromosomes also contain DNA-bound proteins, which serve to package the DNA and control its functions.Chromosomes...
which are inherited together because of close genetic linkage
Genetic linkage
Genetic linkage is the tendency of certain loci or alleles to be inherited together. Genetic loci that are physically close to one another on the same chromosome tend to stay together during meiosis, and are thus genetically linked.-Background:...
and are functionally related in an evolutionary sense, although they are rarely co-regulated genetically.
Supergenes have cis-effect
Cis-regulatory element
A cis-regulatory element or cis-element is a region of DNA or RNA that regulates the expression of genes located on that same molecule of DNA . This term is constructed from the Latin word cis, which means "on the same side as". These cis-regulatory elements are often binding sites for one or...
s due to multiple loci
Locus (genetics)
In the fields of genetics and genetic computation, a locus is the specific location of a gene or DNA sequence on a chromosome. A variant of the DNA sequence at a given locus is called an allele. The ordered list of loci known for a particular genome is called a genetic map...
(which may be within a gene, or within a single gene's regulatory region), and tight linkage. They are classically polymorphic
Polymorphism (biology)
Polymorphism in biology occurs when two or more clearly different phenotypes exist in the same population of a species — in other words, the occurrence of more than one form or morph...
, and different elements code for different fitness effects which combine to form a coherent or epistatic
Epistasis
In genetics, epistasis is the phenomenon where the effects of one gene are modified by one or several other genes, which are sometimes called modifier genes. The gene whose phenotype is expressed is called epistatic, while the phenotype altered or suppressed is called hypostatic...
whole. The two classic supergenes are (1) the Primula
Primula
Primula is a genus of 400–500 species of low-growing herbs in the family Primulaceae. They include primrose, auricula, cowslip and oxlip. Many species are grown for their ornamental flowers...
heterostyly
Heterostyly
Heterostyly is a unique form of polymorphism and herkogamy in flowers. In a heterostylous species, two or three different morphological types of flowers, termed morphs, exist in the population. On each individual plant, all flowers share the same morph. The flower morphs differ in the lengths of...
locus, which controls "pin" and "thrum" types, and (2) the locus controlling Batesian mimetic
Batesian mimicry
Batesian mimicry is a form of mimicry typified by a situation where a harmless species has evolved to imitate the warning signals of a harmful species directed at a common predator...
polymorphism in Papilio memnon
Papilio memnon
The Great Mormon is a large butterfly that belongs to the swallowtail family and is found in southern Asia. It is widely distributed and has thirteen subspecies...
butterflies. For example, pin and thrum morphs of Primula have effects on genetic compatibility (pin style x thrum pollen
Pollen
Pollen is a fine to coarse powder containing the microgametophytes of seed plants, which produce the male gametes . Pollen grains have a hard coat that protects the sperm cells during the process of their movement from the stamens to the pistil of flowering plants or from the male cone to the...
, or thrum style x pin pollen matings are successful, while pin x pin, and thrum x thrum matings are rarely successful due to pollen-style incompatibility
Self-incompatibility in plants
Self-incompatibility is a general name for several genetic mechanisms in angiosperms, which prevent self-fertilization and thus encourage outcrossing...
), and have different style length, anther height in the corolla tube, pollen size, and papilla size on the stigma. Each of these effects is controlled by a different locus in the same supergene, but recombinants are occasionally found with traits combining those of "pin" and "thrum" morphs.
Gene complexes, in contrast, are simply tightly linked groups of genes, often created via gene duplication
Gene duplication
Gene duplication is any duplication of a region of DNA that contains a gene; it may occur as an error in homologous recombination, a retrotransposition event, or duplication of an entire chromosome.The second copy of the gene is often free from selective pressure — that is, mutations of it have no...
(sometimes called segmental duplication
Segmental duplication
Segmental duplications are segments of DNA with near-identical sequence.Segmental duplications give rise to low copy repeats and are believed to have played a role in creating new primate genes as reflected in human genetic variation...
if the duplicates remain side-by-side). Here, each gene has similar though slightly diverged function. For example, the human major histocompatibility complex (MHC)
Major histocompatibility complex
Major histocompatibility complex is a cell surface molecule encoded by a large gene family in all vertebrates. MHC molecules mediate interactions of leukocytes, also called white blood cells , which are immune cells, with other leukocytes or body cells...
region is a complex of tightly linked genes all acting in the immune system, but has no claim to be a supergene, even though the component genes very likely have epistatic effects and are in strong disequilibrium due in part to selection.
No supergene has yet been characterized to the functional DNA
DNA
Deoxyribonucleic acid is a nucleic acid that contains the genetic instructions used in the development and functioning of all known living organisms . The DNA segments that carry this genetic information are called genes, but other DNA sequences have structural purposes, or are involved in...
level, but work is proceeding in a number of species.
The earliest use of the term "supergene" may be in an article by A. Ernst (1936) in the journal Archiv der Julzus Klaus-stiftung fur Vererbungsforschung, Sozialanthropologie und Rassenhygiene.
Origin of supergenes
Classically, supergenes were hypothesized to have evolved from less tightly-linked genes coming together via chromosomal rearrangement or reduced crossing overChromosomal crossover
Chromosomal crossover is an exchange of genetic material between homologous chromosomes. It is one of the final phases of genetic recombination, which occurs during prophase I of meiosis in a process called synapsis. Synapsis begins before the synaptonemal complex develops, and is not completed...
, due to selection for particular multilocus phenotype
Phenotype
A phenotype is an organism's observable characteristics or traits: such as its morphology, development, biochemical or physiological properties, behavior, and products of behavior...
s. For instance, in Batesian mimicry supergenes in species such as Papilio memnon, genes are required to affect hind-wing, fore-wing, and body colour, and also the presence or absence of long projections (the "tails" of swallowtail butterflies).
The case for the accumulative origin for supergenes was originally based on the work of Nabours on polymorphism
Polymorphism (biology)
Polymorphism in biology occurs when two or more clearly different phenotypes exist in the same population of a species — in other words, the occurrence of more than one form or morph...
for colour and pattern in Grouse Locusts (Tetrigidae). In Acridium arenosum the colour-patterns are controlled by thirteen genes on the same chromosome, which reassort (recombine) fairly easily. They also occur in Apotettix eurycephalus where they form two tightly linked groups, between which there is 7% crossing-over. Furthermore, in Paratettix texanus there appears to be complete suppression of crossing-over among 24 out of 25 of the colour-pattern genes, which can be distinguished by comparing their effects with those found in other species. Analysis of Nabour's data by Darlington & Mather
Kenneth Mather
Sir Kenneth Mather FRS was a British geneticist. He was elected a Fellow of the Royal Society in 1949, and won its Darwin Medal in 1964....
concluded that the genes responsible for the morphs of Paratettix texanus have been gradually aggregated into a group which acts as a single switch-mechanism. This explanation was accepted by E.B. Ford
E.B. Ford
Edmund Brisco "Henry" Ford FRS Hon. FRCP was a British ecological geneticist. He was a leader among those British biologists who investigated the role of natural selection in nature. As a schoolboy Ford became interested in lepidoptera, the group of insects which includes butterflies and moths...
and incorporated into his accounts of ecological genetics.
This process might involve suppression of crossing-over, translocation of chromosome fragments and possibly occasional cistron duplication. That crossing-over can be suppressed by selection has been known for many years; Detlefsen and Roberts were able to reduce recombination between the loci for white eyes (w) and miniature wings (m) in Drosophila melanogaster from the normal 36% to 6% in one line and 0.6% in another.
Debate has tended to centre round the question, could the component genes in a super-gene have started off on separate chromosomes, with subsequent reorganization, or is it necessary for them to start on the same chromosome? Many scientists today believe the latter, because some linkage disequilibrium
Linkage disequilibrium
In population genetics, linkage disequilibrium is the non-random association of alleles at two or more loci, not necessarily on the same chromosome. It is also referred to as to as gametic phase disequilibrium , or simply gametic disequilibrium...
is initially needed to select for tighter linkage, and linkage disequilibrium requires both the previous existence of polymorphisms via some other process, like natural selection, favouring gene combinations. If genes are weakly linked, it is probable that the rarer advantageous haplotype
Haplotype
A haplotype in genetics is a combination of alleles at adjacent locations on the chromosome that are transmitted together...
dies out, leading to the loss of polymorphism at the other locus.
Most people, following J.R.G. Turner, therefore argue that supergenes arose in situ due to selection for correlated and epistatic traits, which just happened to have been possible to select via the existence of suitable loci closely linked to the original variant. Turner calls this a "sieve" explanation, and the Turner explanation might be called the "Turner sieve" hypothesis. Maynard Smith
John Maynard Smith
John Maynard Smith,His surname was Maynard Smith, not Smith, nor was it hyphenated. F.R.S. was a British theoretical evolutionary biologist and geneticist. Originally an aeronautical engineer during the Second World War, he took a second degree in genetics under the well-known biologist J.B.S....
agreed with this view in his authoritative textbook. Nevertheless, the question is not definitively settled. The problem is connected to an even larger question, the evolution of evolvability
Evolvability
Evolvability is defined as the capacity of a system for adaptive evolution. Evolvability is the ability of a population of organisms to not merely generate genetic diversity, but to generate adaptive genetic diversity, and thereby evolve through natural selection.In order for a biological organism...
.