Butterfly genome reveals promiscuous exchange of mimicry adaptations among species

James Mallet(Evolutionary Genomics (United States)), Neil Rosser(Minnesota Zoo), Kanchon K. Dasmahapatra(University of California, Irvine), Camilo Salazar(Smithsonian Tropical Research Institute), Nicola J. Nadeau(University of Cambridge), Alison K. Surridge(University of Cambridge), Simon H. Martin(University of Cambridge), Simon W. Baxter(European Bioinformatics Institute), Chris D. Jiggins(Smithsonian Tropical Research Institute), James R. Walters(University of Cambridge), Furong Yuan(University of California, Irvine), Adriana D. Briscoe(University of California, Irvine), Robert D. Reed(University of California, Irvine), James J. Lewis(University of California, Irvine), Arnaud Martin(University of California, Irvine), John W. Davey(Minnesota Zoo),  Mark L. Blaxter(Centre for Immunity, Infection and Evolution), Annabel Whibley(Centre National de la Recherche Scientifique), Mathieu Joron(Centre National de la Recherche Scientifique), Robert T. Jones(Centre National de la Recherche Scientifique), James A. Yorke(University of Maryland, College Park), Aleksey V. Zimin(University of Maryland, College Park), Paul Kersey(European Bioinformatics Institute), Daniel Lawson(European Bioinformatics Institute), Derek A. Wilson(European Bioinformatics Institute), Daniel Hughes(European Bioinformatics Institute), Peter W. H. Holland(University of Oxford), Laura Ferguson(University of Oxford), Camilo Salazar(Smithsonian Tropical Research Institute), W. Owen McMillan(Smithsonian Tropical Research Institute), Chris D. Jiggins(Smithsonian Tropical Research Institute), Sebastian Adler(Universitätsmedizin Greifswald), Katharina J. Hoff(European Bioinformatics Institute), Seung‐Joon Ahn(Max Planck Institute for Chemical Ecology), Yannick Pauchet(Max Planck Institute for Chemical Ecology), David G. Heckel(Max Planck Institute for Chemical Ecology), Heiko Vogel(Max Planck Institute for Chemical Ecology), Dean A. Baker(Imperial College London), Nicola Chamberlain(Harvard University), Marcus R. Kronforst(Harvard University), Ayşe Tenger‐Trolander(Harvard University), Richard H. ffrench‐Constant(University of Exeter), Ritika Chauhan(University of Exeter), Brian A. Counterman(Mississippi State University), Tamás Dalmay(University of East Anglia), Lawrence E. Gilbert(Minnesota Zoo), Alexie Papanicolaou(Ecosystem Sciences), Karl Gordon(Ecosystem Sciences), Heather M. Hines(North Carolina State University), Emmanuelle Jacquin‐Joly(European Bioinformatics Institute), William J. Palmer(University of Cambridge), Francis M. Jiggins(University of California, Irvine), Durrell D. Kapan(University of Hawaiʻi at Mānoa), Durrell D. Kapan(University of Hawaiʻi at Mānoa), Gerardo Lamas(National University of San Marcos), Daniel Mapleson(University of East Anglia), Luana S. Maroja(Williams College), Simon Moxon(Yale University), Riccardo Papa(University of Puerto Rico at Río Piedras), David A. Ray(Mississippi State University), David A. Ray(Mississippi State University), Steven L. Salzberg(Johns Hopkins University), Megan A. Supple(North Carolina State University), Paul A. Wilkinson(University of Bristol),  Mark L. Blaxter(Centre for Immunity, Infection and Evolution), Alexi L. Balmuth(Edinburgh Genomics), Karim Gharbi(Edinburgh Genomics), Marian Thomson(Edinburgh Genomics), Cathlene Eland(Edinburgh Genomics), Stephen Richards(Baylor College of Medicine), Lingling Pu(Baylor College of Medicine), Steven E. Scherer(Baylor College of Medicine), Christie Kovar(Baylor College of Medicine), Tittu Mathew(Baylor College of Medicine), Kim C. Worley(Baylor College of Medicine), Rebecca Thornton(Baylor College of Medicine), Donna M. Muzny(Baylor College of Medicine), Yuanqing Wu(Baylor College of Medicine), Yi Han(Baylor College of Medicine), Fiona Ongeri(Baylor College of Medicine), Joy C. Jayaseelan(Baylor College of Medicine), Jiaxin Qu(Baylor College of Medicine), Richard A. Gibbs(Baylor College of Medicine), Mauricio Linares(Universidad de Los Andes), Sean P. Mullen(Boston University), James Mallet(Evolutionary Genomics (United States))
Nature
May 15, 2012
Cited by 1,294Open Access
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Abstract

Sequencing of the genome of the butterfly Heliconius melpomene shows that closely related Heliconius species exchange protective colour-pattern genes promiscuously. Heliconius butterflies are an excellent system in which to study ecology, behaviour, mimicry and speciation. The genome of the postman butterfly Heliconius melpomene has now been sequenced. Using genomic resequencing of individuals from distinct lineages, the authors document heterogenous patterns of genomic diversity associated with adaptively divergent wing-colour patterns. As the second lepidopteran genome to be sequenced, Heliconius offers novel opportunities for comparative genomics within this economically significant insect order, which includes many pest species, as well as the only domesticated insect, the silkmoth Bombyx mori. The evolutionary importance of hybridization and introgression has long been debated1. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation2,3,4,5. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12,669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation.


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