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      A genetic mechanism for female-limited Batesian mimicry in Papilio butterfly.

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          Abstract

          In Batesian mimicry, animals avoid predation by resembling distasteful models. In the swallowtail butterfly Papilio polytes, only mimetic-form females resemble the unpalatable butterfly Pachliopta aristolochiae. A recent report showed that a single gene, doublesex (dsx), controls this mimicry; however, the detailed molecular mechanisms remain unclear. Here we determined two whole-genome sequences of P. polytes and a related species, Papilio xuthus, identifying a single ∼130-kb autosomal inversion, including dsx, between mimetic (H-type) and non-mimetic (h-type) chromosomes in P. polytes. This inversion is associated with the mimicry-related locus H, as identified by linkage mapping. Knockdown experiments demonstrated that female-specific dsx isoforms expressed from the inverted H allele (dsx(H)) induce mimetic coloration patterns and simultaneously repress non-mimetic patterns. In contrast, dsx(h) does not alter mimetic patterns. We propose that dsx(H) switches the coloration of predetermined wing patterns and that female-limited polymorphism is tightly maintained by chromosomal inversion.

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          Most cited references13

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          LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA.

          To compare entire genomes from different species, biologists increasingly need alignment methods that are efficient enough to handle long sequences, and accurate enough to correctly align the conserved biological features between distant species. We present LAGAN, a system for rapid global alignment of two homologous genomic sequences, and Multi-LAGAN, a system for multiple global alignment of genomic sequences. We tested our systems on a data set consisting of greater than 12 Mb of high-quality sequence from 12 vertebrate species. All the sequence was derived from the genomic region orthologous to an approximately 1.5-Mb region on human chromosome 7q31.3. We found that both LAGAN and Multi-LAGAN compare favorably with other leading alignment methods in correctly aligning protein-coding exons, especially between distant homologs such as human and chicken, or human and fugu. Multi-LAGAN produced the most accurate alignments, while requiring just 75 minutes on a personal computer to obtain the multiple alignment of all 12 sequences. Multi-LAGAN is a practical method for generating multiple alignments of long genomic sequences at any evolutionary distance. Our systems are publicly available at http://lagan.stanford.edu.
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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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              Development, plasticity and evolution of butterfly eyespot patterns.

              The developmental and genetic bases for the formation, plasticity and diversity of eyespot patterns in butterflies are examined. Eyespot pattern mutants, regulatory gene expression, and transplants of the eyespot developmental organizer demonstrate that eyespot position, number, size and colour are determined progressively in a developmental pathway largely uncoupled from those regulating other wing-pattern elements and body structures. Species comparisons and selection experiments suggest that the evolution of eyespot patterns can occur rapidly through modulation of different stages of this pathway, and requires only single, or very few, changes in regulatory genes.
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                Author and article information

                Journal
                Nat. Genet.
                Nature genetics
                1546-1718
                1061-4036
                Apr 2015
                : 47
                : 4
                Affiliations
                [1 ] Department of Integrated Biosciences, University of Tokyo, Kashiwa, Japan.
                [2 ] Department of Biological Information, Tokyo Institute of Technology, Meguro-ku, Japan.
                [3 ] 1] Department of Integrated Biosciences, University of Tokyo, Kashiwa, Japan. [2] Laboratory for Morphogenetic Signaling, RIKEN Center for Developmental Biology, Kobe, Japan.
                [4 ] Department of Computational Biology, University of Tokyo, Kashiwa, Japan.
                [5 ] Department of Medical Genome Sciences, University of Tokyo, Kashiwa, Japan.
                [6 ] 1] Center for Information Biology, National Institute of Genetics, Mishima, Japan. [2] Principle of Informatics, National Institute of Informatics, Chiyoda-ku, Japan.
                [7 ] Kazusa DNA Research Institute, Kisarazu, Japan.
                [8 ] JT Biohistory Research Hall, Takatsuki, Japan.
                [9 ] Center for Gene Research, Nagoya University, Nagoya, Japan.
                Article
                ng.3241
                10.1038/ng.3241
                25751626
                6d30cacd-4988-4d03-a9c6-75cc19d5275f
                History

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