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 phenotypes1. Polymorphic supergenes, in which specific combinations of traits are maintained within a single population, were first described for ‘pin’ and ‘thrum’ floral types in Primula1 and Fagopyrum2, but classic examples are also found in insect mimicry3,4,5 and snail morphology6. 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 challenge7,8,9,10. 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 species9,10,11, 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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Figure 1: Supergene alleles and mimicry polymorphism in H. numata.
Figure 2: Fine-scale mapping and nucleotide variation at the P supergene in H. numata.
Figure 3: Chromosomal rearrangements associated with the supergene in natural populations.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

GenBank accessions for BAC clone sequences: FP885863, FP476061, FP565803, FP476023, CU856181, FP885878, FP476047, FP885857, CU856182, CU655868, FP885879, FP885861, FP885880, FP885855, CU914733, FP475989, CU655869, CU914734, CU633161, CU638865, CU856175, FP884220 and FP236755. Accessions for 1364 marker sequences: JN173798–JN175161.

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Acknowledgements

We thank M. Blaxter and D. Charlesworth for advice throughout the study; The GenePool and S. Humphray for DNA sequencing; S. Kumar and A. Papanicolaou for bioinformatics support; M. Beltrán, A. Bulski, M. Veuille and the Botanique-Entomologie-Mycologie molecular facility (BoEM) for laboratory support; S. Johnston for genome-size estimates in H. numata; D. Obbard for providing R scripts; M. Abanto, S. Gallusser, C. Ramírez, L. de Silva, J. Barbut, B. Gilles and G. Lamas for help with butterfly rearing, fieldwork and collecting permits; and the Peruvian National Institute of Natural Resources (INRENA) for granting collecting and export permits (076-2007-INRENA-IFFS-DCB). Fieldwork in French Guiana was supported by a CNRS ‘Nouragues Research Grant’. This work was supported by an EMBO long-term fellowship (ALTF-431-2004), EMBO-matching funds from NWO (Netherlands), a Royal Society University Research Fellowship (516002.K5917/ROG), a CNRS grant (ATIP Biodiversité 2008, France) and a European Research Council Starting Grant (ERC-Stg ‘MimEvol’) to M.J., a BBSRC grant (BBE0118451) to C.D.J. and R.H.ff.-C., a Leverhulme Trust grant (F/00144AY) to R.H.ff.-C., and a Royal Society University Research Fellowship and a Leverhulme Research Leadership grant to C.D.J.

Author information

M.J., C.D.J. and R.H.ff.-C. designed the study and contributed to all stages of the project. M.J., L. Frezal and R.T.J. performed the principal experiments and data analysis, with assistance from N.L.C., S.W.B., S.F.L., M.B., C.S., L. Ferguson, C.R.H., A.W. and P.A.W. BAC clone sequencing was carried out by C.D., R.G., C.L., R.C., H.B., S.S., J.R., M.C.J. and M.A.Q. M.J., A.W., C.D.J. and R.H.ff.-C. co-wrote the manuscript with input from all authors.

Correspondence to Mathieu Joron.

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Joron, M., Frezal, L., Jones, R. et al. Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477, 203–206 (2011). https://doi.org/10.1038/nature10341

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