Supergene

Supergene

A supergene is a group of neighbouring genes 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. [cite journal |author=Joron M, Papa R, Beltrán M, "et al" |title=A conserved supergene locus controls colour pattern diversity in Heliconius butterflies |journal=PLoS Biol. |volume=4 |issue=10 |pages=e303 |year=2006 |pmid=17002517 |url=http://biology.plosjournals.org/perlserv/?request=get-document&doi=10.1371/journal.pbio.0040303 |doi=10.1371/journal.pbio.0040303]

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, 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 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. [Ernst A. 1936. Weitere Untersuchungen zur Phänanalyse, zum Fertilitätsproblem und zur Genetik heterostyler Primeln. II. "Primula hortensis". Wettst. Arch. J. K.-Stift. Ver. Sozialanthropol. Ras. 11, 1-280.]

Origin of supergenes

Classically, supergenes were hypothesized to have evolved from less tightly-linked genes coming together via chromosomal rearrangement or reduced crossing over, due to selection for particular multilocus phenotypes. 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. [Nabours R.K. 1929. The genetics of the Tettigidae [Tetrigidae] (Grouse Locusts). "Bibliogr. genet." 5, 27-104.] [Nabours R.K., Larson L. & Hartwig N. 1933. Inheritance of colour-patterns in the grouse-locust "Acridium arenosum" Burmeister (Tettigidae [Tetrigidae] . "Genetics" 18, 159-71.] [Darlington C.D. & Mather K. 1949. "The elements of genetics", p335-6. Allen & Unwin, London.] This explanation was accepted by E.B. Ford and incorporated into his accounts of ecological genetics. [Ford E.B. 1965. "Genetic polymorphism", p17-25. MIT Press 1965.] [Ford E.B. 1975. "Ecological genetics". 4th ed, Chapman & Hall. London.]

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 reduce recombination between the loci for white eyes (w) and mimiature wings (m) in "Drosophila melanogaster" from the normal 36% to 6% in one line and 0.6% in another. [Detlefsen J.A. and Roberts E. 1921. Studies on crossing-over I. The effects of selection on crossover values. "J Exp Zoology". 32, 333-54.] [Darlington C.D. 1956. "Chromosome botany", p36. Allen & Unwin, London.]

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. [Charlesworth D. and Charlesworth B. 1975. Theoretical genetics of Batesian mimicry I. Single-locus models. "J. Theoret. Biol." 55, 283-303; II. Evolution of supergenes. "J. Theoret. Biol." 55, 305-324; III. Evolution of dominance. "J. Theoret. Biol." 55, 325-337.] 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 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. [Turner JRG 1984. Mimicry: the palatability spectrum and its consequences. Chap. 14. In Vane-Wright R.I. & Ackery P.R. (eds) "The Biology of Butterflies". Symposia of the Royal Entomological Society ofLondon #11. Academic Press, London.] Maynard Smith agreed with this view in his authoritative textbook. [Maynard Smith J. 1998. "Evolutionary genetics", 2nd ed. Oxford.] Nevertheless, the question is not definitively settled.

References


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