Genome-wide evidence for speciation with gene flow in Heliconius butterflies

  1. Chris D. Jiggins1
  1. 1Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom;
  2. 2Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, United Kingdom;
  3. 3Department of Biology, University of York, York YO10 5DD, United Kingdom;
  4. 4Facultad de Ciencias Naturales y Matematicas, Universidad del Rosario, Bogota DC, Colombia;
  5. 5Department of Biology, Stanford University, Stanford, California 94305, USA;
  6. 6Institute of Evolutionary Biology, The University of Edinburgh, Edinburgh EH9 3JT, United Kingdom;
  7. 7Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA

    Abstract

    Most speciation events probably occur gradually, without complete and immediate reproductive isolation, but the full extent of gene flow between diverging species has rarely been characterized on a genome-wide scale. Documenting the extent and timing of admixture between diverging species can clarify the role of geographic isolation in speciation. Here we use new methodology to quantify admixture at different stages of divergence in Heliconius butterflies, based on whole-genome sequences of 31 individuals. Comparisons between sympatric and allopatric populations of H. melpomene, H. cydno, and H. timareta revealed a genome-wide trend of increased shared variation in sympatry, indicative of pervasive interspecific gene flow. Up to 40% of 100-kb genomic windows clustered by geography rather than by species, demonstrating that a very substantial fraction of the genome has been shared between sympatric species. Analyses of genetic variation shared over different time intervals suggested that admixture between these species has continued since early in speciation. Alleles shared between species during recent time intervals displayed higher levels of linkage disequilibrium than those shared over longer time intervals, suggesting that this admixture took place at multiple points during divergence and is probably ongoing. The signal of admixture was significantly reduced around loci controlling divergent wing patterns, as well as throughout the Z chromosome, consistent with strong selection for Müllerian mimicry and with known Z-linked hybrid incompatibility. Overall these results show that species divergence can occur in the face of persistent and genome-wide admixture over long periods of time.

    Footnotes

    • Received April 23, 2013.
    • Accepted August 15, 2013.

    This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 3.0 Unported), as described at http://creativecommons.org/licenses/by-nc/3.0/.

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