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      The status of supergenes in the 21st century: recombination suppression in Batesian mimicry and sex chromosomes and other complex adaptations

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          Abstract

          I review theoretical models for the evolution of supergenes in the cases of Batesian mimicry in butterflies, distylous plants and sex chromosomes. For each of these systems, I outline the genetic evidence that led to the proposal that they involve multiple genes that interact during ‘complex adaptations’, and at which the mutations involved are not unconditionally advantageous, but show advantages that trade‐off against some disadvantages. I describe recent molecular genetic studies of these systems and questions they raise about the evolution of suppressed recombination. Nonrecombining regions of sex chromosomes have long been known, but it is not yet fully understood why recombination suppression repeatedly evolved in systems in distantly related taxa, but does not always evolve. Recent studies of distylous plants are tending to support the existence of recombination‐suppressed genome regions, which may include modest numbers of genes and resemble recently evolved sex‐linked regions. For Batesian mimicry, however, molecular genetic work in two butterfly species suggests a new supergene scenario, with a single gene mutating to produce initial adaptive phenotypes, perhaps followed by modifiers specifically refining and perfecting the new phenotype.

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          A test of neutral molecular evolution based on nucleotide data.

          The neutral theory of molecular evolution predicts that regions of the genome that evolve at high rates, as revealed by interspecific DNA sequence comparisons, will also exhibit high levels of polymorphism within species. We present here a conservative statistical test of this prediction based on a constant-rate neutral model. The test requires data from an interspecific comparison of at least two regions of the genome and data on levels of intraspecific polymorphism in the same regions from at least one species. The model is rejected for data from the region encompassing the Adh locus and the 5' flanking sequence of Drosophila melanogaster and Drosophila sechellia. The data depart from the model in a direction that is consistent with the presence of balanced polymorphism in the coding region.
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            Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry.

            Supergenes are tight clusters of loci that facilitate the co-segregation of adaptive variation, providing integrated control of complex adaptive phenotypes. Polymorphic supergenes, in which specific combinations of traits are maintained within a single population, were first described for 'pin' and 'thrum' floral types in Primula and Fagopyrum, but classic examples are also found in insect mimicry and snail morphology. Understanding the evolutionary mechanisms that generate these co-adapted gene sets, as well as the mode of limiting the production of unfit recombinant forms, remains a substantial challenge. Here we show that individual wing-pattern morphs in the polymorphic mimetic butterfly Heliconius numata are associated with different genomic rearrangements at the supergene locus P. These rearrangements tighten the genetic linkage between at least two colour-pattern loci that are known to recombine in closely related species, with complete suppression of recombination being observed in experimental crosses across a 400-kilobase interval containing at least 18 genes. In natural populations, notable patterns of linkage disequilibrium (LD) are observed across the entire P region. The resulting divergent haplotype clades and inversion breakpoints are found in complete association with wing-pattern morphs. Our results indicate that allelic combinations at known wing-patterning loci have become locked together in a polymorphic rearrangement at the P locus, forming a supergene that acts as a simple switch between complex adaptive phenotypes found in sympatry. These findings highlight how genomic rearrangements can have a central role in the coexistence of adaptive phenotypes involving several genes acting in concert, by locally limiting recombination and gene flow.
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              The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database.

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                Author and article information

                Journal
                Evol Appl
                Evol Appl
                10.1111/(ISSN)1752-4571
                EVA
                Evolutionary Applications
                John Wiley and Sons Inc. (Hoboken )
                1752-4571
                06 August 2015
                January 2016
                : 9
                : 1 , Women's contribution to basic and applied evolutionary biology ( doiID: 10.1111/eva.2016.9.issue-1 )
                : 74-90
                Affiliations
                [ 1 ] Institute of Evolutionary BiologyUniversity of Edinburgh EdinburghUK
                Author notes
                [*] [* ] Correspondence

                Deborah Charlesworth, Institute of Evolutionary Biology, University of Edinburgh, Ashworth Lab. King's Buildings, W. Mains Rd., Edinburgh EH9 3FL, UK.

                Tel.: +44‐131‐6505751;

                fax: +44‐131‐6506564;

                e‐mail: Deborah.Charlesworth@ 123456ed.ac.uk

                Article
                EVA12291
                10.1111/eva.12291
                4780387
                27087840
                f915be06-98cf-4511-bdf1-d54296ceb6af
                © 2015 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 24 February 2015
                : 16 June 2015
                Page count
                Pages: 17
                Funding
                Funded by: Leverhulme Trust
                Categories
                Original Article
                Original Article
                Custom metadata
                2.0
                eva12291
                January 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.8.4 mode:remove_FC converted:07.03.2016

                Evolutionary Biology
                batesian mimicry,distyly,recombination suppression,sex chromosomes,sex‐limited expression

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