A supergene is a
chromosomal region encompassing multiple neighboring
gene
In biology, the word gene (from , ; "... Wilhelm Johannsen coined the word gene to describe the Mendelian units of heredity..." meaning ''generation'' or ''birth'' or ''gender'') can have several different meanings. The Mendelian gene is a b ...
s that are inherited together because of close
genetic linkage, i.e. much less recombination than would normally be expected.
This mode of inheritance can be due to genomic rearrangements between supergene variants.
A supergene region can contain few, functionally related genes that clearly contribute to a shared phenotype.
Phenotypes encoded by supergenes
Supergenes have
cis-effects 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, whereby different supergene variants code for different phenotypes.
Classic supergenes include many
sex chromosome
A sex chromosome (also referred to as an allosome, heterotypical chromosome, gonosome, heterochromosome, or idiochromosome) is a chromosome that differs from an ordinary autosome in form, size, and behavior. The human sex chromosomes, a typical ...
s, the ''
Primula
''Primula'' () is a genus of herbaceous flowering plants in the family Primulaceae. They include the primrose ('' P. vulgaris''), a familiar wildflower of banks and verges. Other common species are '' P. auricula'' (auricula), '' P. veris'' (cow ...
''
heterostyly
Heterostyly is a unique form of polymorphism and herkogamy in flowers. In a heterostylous species, two or three morphological types of flowers, termed "morphs", exist in the population. On each individual plant, all flowers share the same morph ...
locus, which controls "
pin
A pin is a device used for fastening objects or material together.
Pin or PIN may also refer to:
Computers and technology
* Personal identification number (PIN), to access a secured system
** PIN pad, a PIN entry device
* PIN, a former Dutch ...
" and "
thrum" types, and the locus controlling
Batesian mimetic polymorphism in ''
Papilio memnon
''Papilio memnon'', the great Mormon, is a large butterfly native to southern Asia that belongs to the swallowtail family. It is widely distributed and has thirteen subspecies. The female is polymorphic and with mimetic forms.
Range
Its rang ...
'' butterflies. Recently discovered supergenes are responsible complex phenotypes including color-morphs in the
white-throated sparrow
The white-throated sparrow (''Zonotrichia albicollis'') is a passerine bird of the New World sparrow family Passerellidae.
Etymology
The genus name ''Zonotrichia'' is from Ancient Greek (, ) and (, ). The specific ''albicollis'' is from Lati ...
.
Primula supergene. Pin and thrum morphs of Primula have effects on genetic compatibility (pin
style
Style is a manner of doing or presenting things and may refer to:
* Architectural style, the features that make a building or structure historically identifiable
* Design, the process of creating something
* Fashion, a prevailing mode of clothing ...
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.
Origin
The earliest use of the term "supergene" may be in an article by A. Ernst (1936) in the journal Archiv der Julius Klaus-Stiftung für Vererbungsforschung, Sozialanthropologie und Rassenhygiene.
Classically, supergenes were hypothesized to have evolved from less tightly-linked genes coming together via
chromosomal rearrangement
In genetics, a chromosomal rearrangement is a mutation that is a type of chromosome abnormality involving a change in the structure of the native chromosome. Such changes may involve several different classes of events, like deletions, duplica ...
or reduced
crossing over, due to selection for particular multilocus
phenotype
In genetics, the phenotype () is the set of observable characteristics or traits of an organism. The term covers the organism's morphology or physical form and structure, its developmental processes, its biochemical and physiological pr ...
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
Edmund Brisco "Henry" Ford (23 April 1901 – 2 January 1988) 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 i ...
and incorporated into his accounts of ecological genetics.
This process might involve suppression of crossing-over,
translocation of chromosome fragments and possibly occasional
cistron
A cistron is an alternative term for "gene". The word cistron is used to emphasize that genes exhibit a specific behavior in a cis-trans test; distinct positions (or loci) within a genome are cistronic.
History
The words ''cistron'' and ''gene ...
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
In population genetics, linkage disequilibrium (LD) is the non-random association of alleles at different loci in a given population. Loci are said to be in linkage disequilibrium when the frequency of association of their different alleles is h ...
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
John Maynard Smith (6 January 1920 – 19 April 2004) was a British theoretical and mathematical evolutionary biologist and geneticist. Originally an aeronautical engineer during the Second World War, he took a second degree in genetics und ...
agreed with this view in his authoritative textbook.
[ Maynard Smith J. 1998. ''Evolutionary genetics'', 2nd ed. Oxford.] Nevertheless, the question is not definitively settled. The problem is connected to an even larger question, the evolution of
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 throu ...
.
Genomic structure
Genomic rearrangements such as inversions can suppress recombination.
Suppressed recombination leads to accumulation of repetitive elements (including to degenerative expansion in early supergene evolution
ef Papaya, Fire ant and to changes in gene expression
ef Fire ant, anther smut
Gene complexes are not supergenes
Gene complexes, in contrast, are simply tightly linked groups of genes, often created via
gene duplication (sometimes called
tandem 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.
References
{{reflist
Reading
Berdan EL, Flatt T, Kozak
GM, Lotterhos KE, Wielstra B. 2022 Genomic
architecture of supergenes: connecting form
and function. Phil. Trans. R. Soc. B 377:
20210192
External links
www.cbc.yale.edu/old/cce/papers/HomNat/homnat.html- evolution of modularity
Genes