title: Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry.
abstract: 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.
authors.affiliation: CNRS UMR 7205, Muséum National d'Histoire Naturelle, CP50, 45 Rue Buffon, 75005 Paris, France. joron@mnhn.fr
authors.forename: Mathieu
authors.initials: M
authors.lastname: Joron
authors.forename: Lise
authors.initials: L
authors.lastname: Frezal
authors.forename: Robert T
authors.initials: RT
authors.lastname: Jones
authors.forename: Nicola L
authors.initials: NL
authors.lastname: Chamberlain
authors.forename: Siu F
authors.initials: SF
authors.lastname: Lee
authors.forename: Christoph R
authors.initials: CR
authors.lastname: Haag
authors.forename: Annabel
authors.initials: A
authors.lastname: Whibley
authors.forename: Michel
authors.initials: M
authors.lastname: Becuwe
authors.forename: Simon W
authors.initials: SW
authors.lastname: Baxter
authors.forename: Laura
authors.initials: L
authors.lastname: Ferguson
authors.forename: Paul A
authors.initials: PA
authors.lastname: Wilkinson
authors.forename: Camilo
authors.initials: C
authors.lastname: Salazar
authors.forename: Claire
authors.initials: C
authors.lastname: Davidson
authors.forename: Richard
authors.initials: R
authors.lastname: Clark
authors.forename: Michael A
authors.initials: MA
authors.lastname: Quail
authors.forename: Helen
authors.initials: H
authors.lastname: Beasley
authors.forename: Rebecca
authors.initials: R
authors.lastname: Glithero
authors.forename: Christine
authors.initials: C
authors.lastname: Lloyd
authors.forename: Sarah
authors.initials: S
authors.lastname: Sims
authors.forename: Matthew C
authors.initials: MC
authors.lastname: Jones
authors.forename: Jane
authors.initials: J
authors.lastname: Rogers
authors.forename: Chris D
authors.initials: CD
authors.lastname: Jiggins
authors.forename: Richard H
authors.initials: RH
authors.lastname: ffrench-Constant
mesh_terms: D000483:Alleles; D000818:Animals; D002080:Butterflies / Q000033:anatomy & histology / Q000235:genetics* / Q000502:physiology; D016386:Chromosome Walking; D059006:Chromosomes, Insect / Q000235:genetics*; D015321:Gene Rearrangement / Q000235:genetics*; D017344:Genes, Insect / Q000235:genetics*; D008040:Genetic Linkage / Q000235:genetics; D006239:Haplotypes / Q000235:genetics; D018716:Molecular Mimicry / Q000235:genetics* / Q000502:physiology; D008969:Molecular Sequence Data; D005810:Multigene Family / Q000235:genetics; D010641:Phenotype; D010858:Pigmentation / Q000235:genetics / Q000502:physiology; D011110:Polymorphism, Genetic / Q000235:genetics*; D014921:Wings, Animal / Q000033:anatomy & histology / Q000378:metabolism / Q000502:physiology