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      A Conserved Supergene Locus Controls Colour Pattern Diversity in Heliconius Butterflies

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          Abstract

          We studied whether similar developmental genetic mechanisms are involved in both convergent and divergent evolution. Mimetic insects are known for their diversity of patterns as well as their remarkable evolutionary convergence, and they have played an important role in controversies over the respective roles of selection and constraints in adaptive evolution. Here we contrast three butterfly species, all classic examples of Müllerian mimicry. We used a genetic linkage map to show that a locus, Yb, which controls the presence of a yellow band in geographic races of Heliconius melpomene, maps precisely to the same location as the locus Cr, which has very similar phenotypic effects in its co-mimic H. erato. Furthermore, the same genomic location acts as a “supergene”, determining multiple sympatric morphs in a third species, H. numata. H. numata is a species with a very different phenotypic appearance, whose many forms mimic different unrelated ithomiine butterflies in the genus Melinaea. Other unlinked colour pattern loci map to a homologous linkage group in the co-mimics H. melpomene and H. erato, but they are not involved in mimetic polymorphism in H. numata. Hence, a single region from the multilocus colour pattern architecture of H. melpomene and H. erato appears to have gained control of the entire wing-pattern variability in H. numata, presumably as a result of selection for mimetic “supergene” polymorphism without intermediates. Although we cannot at this stage confirm the homology of the loci segregating in the three species, our results imply that a conserved yet relatively unconstrained mechanism underlying pattern switching can affect mimicry in radically different ways. We also show that adaptive evolution, both convergent and diversifying, can occur by the repeated involvement of the same genomic regions.

          Abstract

          In an intriguing example of adaptive evolution, genetic linkage analysis identifies a conserved region in distantly related Heliconius butterfly species that controls the diverse effects of wing patterning and mimicry.

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          Most cited references52

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          Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles.

          Major phenotypic changes evolve in parallel in nature by molecular mechanisms that are largely unknown. Here, we use positional cloning methods to identify the major chromosome locus controlling armor plate patterning in wild threespine sticklebacks. Mapping, sequencing, and transgenic studies show that the Ectodysplasin (EDA) signaling pathway plays a key role in evolutionary change in natural populations and that parallel evolution of stickleback low-plated phenotypes at most freshwater locations around the world has occurred by repeated selection of Eda alleles derived from an ancestral low-plated haplotype that first appeared more than two million years ago. Members of this clade of low-plated alleles are present at low frequencies in marine fish, which suggests that standing genetic variation can provide a molecular basis for rapid, parallel evolution of dramatic phenotypic change in nature.
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            The ecology of adaptive radiation

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              Evolution of supergene families associated with insecticide resistance.

              The emergence of insecticide resistance in the mosquito poses a serious threat to the efficacy of many malaria control programs. We have searched the Anopheles gambiae genome for members of the three major enzyme families- the carboxylesterases, glutathione transferases, and cytochrome P450s-that are primarily responsible for metabolic resistance to insecticides. A comparative genomic analysis with Drosophila melanogaster reveals that a considerable expansion of these supergene families has occurred in the mosquito. Low gene orthology and little chromosomal synteny paradoxically contrast the easily identified orthologous groups of genes presumably seeded by common ancestors. In A. gambiae, the independent expansion of paralogous genes is mainly a consequence of the formation of clusters among locally duplicated genes. These expansions may reflect the functional diversification of supergene families consistent with major differences in the life history and ecology of these organisms. These data provide a basis for identifying the resistance-associated enzymes within these families. This will enable the resistance status of mosquitoes, flies, and possibly other holometabolous insects to be monitored. The analyses also provide the means for identifying previously unknown molecules involved in fundamental biological processes such as development.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                pbio
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                October 2006
                26 September 2006
                : 4
                : 10
                : e303
                Affiliations
                [1 ] Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
                [2 ] Institute of Biology, Leiden University, Leiden, Netherlands
                [3 ] The Galton Laboratory, Department of Biology, University College London, London, United Kingdom
                [4 ] Department of Biology, University of Puerto Rico, San Juan, Puerto Rico
                [5 ] Department of Biology and Biochemistry, University of Bath, Bath, United Kingdom
                [6 ] Smithsonian Tropical Research Institute, Balboa, Panama
                [7 ] Jirón Alegría Arias de Morey, Tarapoto, Peru
                [8 ] The Wellcome Trust Sanger Institute, Cambridge, United Kingdom
                Duke University, United States of America
                Author notes
                * To whom correspondence should be addressed. E-mail: mathieu.joron@ 123456ed.ac.uk
                Article
                06-PLBI-RA-0613R2 plbi-04-10-10
                10.1371/journal.pbio.0040303
                1570757
                17002517
                1ad30151-6a7f-40cf-bb65-c4e3d3fa2db0
                Copyright: © 2006 Joron et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 12 April 2006
                : 14 July 2006
                Page count
                Pages: 10
                Categories
                Research Article
                Evolution
                Genetics/Genomics/Gene Therapy
                Zoology
                Insects
                Custom metadata
                Joron M, Papa R, Beltrán M, Chamberlain N, Mavárez J, et al. (2006) A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. PLoS Biol 4(10): e303. DOI: 10.1371/journal.pbio.0040303

                Life sciences
                Life sciences

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