Journal Article

doublesex is a mimicry supergene

Palmer, D. H., Martin, A., Kunte, K., Kronforst, M. R., Mullen, S. P., Zhang, W., Tenger-Trolander, A., Reed, R. D.

2014

Overview

The phenomenon of sex-limited mimicry is phylogenetically widespread in the swallowtail butterfly genus Papilio — now, a single gene, doublesex , is shown to control supergene mimicry, a finding that is in contrast to the long-held view that supergenes are likely to be controlled by a tightly linked cluster of loci. How super is a supergene? In some butterfly species one sex — usually the female — mimics the wing pattern of a toxic species. In the 1960s the phenomenon was proposed to be under the control of a 'supergene'. More recently a consensus has emerged that supergenes are likely to be clusters of tightly linked genes, each influencing a different aspect of mimetic wing patterning. Now Marcus Kronforst and colleagues show, surprisingly, that in a classic supergene mimic, the swallowtail butterfly Papilio polytes , the supergene is truly a single gene. And another surprise: that gene is a well-known component in the sex determination pathway called doublesex . Gene expression and DNA sequence variation data suggest that isoform expression differences and protein sequence evolution also contribute to the differences between doublesex mimicry alleles. Thus the P. polytes mimicry supergene can be summed up as a fusion of previous hypotheses: single-gene control but with help from multiple functional mutations. One of the most striking examples of sexual dimorphism is sex-limited mimicry in butterflies, a phenomenon in which one sex—usually the female—mimics a toxic model species, whereas the other sex displays a different wing pattern 1 . Sex-limited mimicry is phylogenetically widespread in the swallowtail butterfly genus Papilio , in which it is often associated with female mimetic polymorphism 1 , 2 , 3 . In multiple polymorphic species, the entire wing pattern phenotype is controlled by a single Mendelian ‘supergene’ 4 . Although theoretical work has explored the evolutionary dynamics of supergene mimicry 5 , 6 , 7 , 8 , 9 , there are almost no empirical data that address the critical issue of what a mimicry supergene actually is at a functional level. Using an integrative approach combining genetic and association mapping, transcriptome and genome sequencing, and gene expression analyses, we show that a single gene, doublesex , controls supergene mimicry in Papilio polytes . This is in contrast to the long-held view that supergenes are likely to be controlled by a tightly linked cluster of loci 4 . Analysis of gene expression and DNA sequence variation indicates that isoform expression differences contribute to the functional differences between dsx mimicry alleles, and protein sequence evolution may also have a role. Our results combine elements from different hypotheses for the identity of supergenes, showing that a single gene can switch the entire wing pattern among mimicry phenotypes but may require multiple, tightly linked mutations to do so.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 38 / 45 / 45/23 / 45/77 / 45/91 / 631/181/2474 / 631/181/2476/2477 / 631/181/457/649/2157 / 631/208/212/748 / 64 / 82 / 82/51 / Alleles / Animals / Artificial chromosomes / Butterflies / Butterflies & moths / Butterflies - anatomy & histology / Butterflies - genetics / Butterflies - physiology / DNA-Binding Proteins / Drosophila Proteins / Evolution, Molecular / Female / Females / Gene Expression Regulation / Genes, Insect / Genomes / Genomics / Humanities and Social Sciences / Hypotheses / Insects / letter / Male / Males / Mimicry (Biology) / Molecular Mimicry - genetics / Molecular Mimicry - physiology / Molecular Sequence Data / multidisciplinary / Mutation - genetics / Phenotype / Physiological aspects / Pigmentation - genetics / Pigmentation - physiology / Polymorphism, Genetic - genetics / Predation (Biology) / Science / Sex Characteristics / Transcriptome - genetics / Wings, Animal - physiology / Zoological research