Genomic architecture and introgression shape a butterfly radiation

Author:

Edelman Nathaniel B.1ORCID,Frandsen Paul B.23ORCID,Miyagi Miriam1,Clavijo Bernardo4ORCID,Davey John56ORCID,Dikow Rebecca B.3ORCID,García-Accinelli Gonzalo4ORCID,Van Belleghem Steven M.7ORCID,Patterson Nick89ORCID,Neafsey Daniel E.910ORCID,Challis Richard11ORCID,Kumar Sujai12ORCID,Moreira Gilson R. P.13,Salazar Camilo14ORCID,Chouteau Mathieu15ORCID,Counterman Brian A.16ORCID,Papa Riccardo717ORCID,Blaxter Mark11ORCID,Reed Robert D.18ORCID,Dasmahapatra Kanchon K.5,Kronforst Marcus19ORCID,Joron Mathieu20ORCID,Jiggins Chris D.6ORCID,McMillan W. Owen21ORCID,Di Palma Federica4,Blumberg Andrew J.22,Wakeley John1,Jaffe David923ORCID,Mallet James1ORCID

Affiliation:

1. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.

2. Department of Plant and Wildlife Sciences, Brigham Young University, Provo, UT 84602, USA.

3. Data Science Lab, Office of the Chief Information Officer, Smithsonian Institution, Washington, DC 20560, USA.

4. Earlham Institute, Norwich Research Park, Norwich NR4 7UZ, UK.

5. Bioscience Technology Facility, Department of Biology, University of York, York YO10 5DD, UK.

6. Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK.

7. Department of Biology, University of Puerto Rico, Río Piedras Campus, San Juan, PR 00931-3360, Puerto Rico.

8. Department of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.

9. Broad Institute of MIT and Harvard, Cambridge, MA, 02142 USA.

10. Harvard TH Chan School of Public Health, Boston, MA 02115, USA.

11. Wellcome Sanger Institute, Wellcome Genome Campus, Cambridge CB10 1SA, UK.

12. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, UK.

13. Departamento de Zoologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, 91501-970 Brasil.

14. Biology Program, Faculty of Natural Sciences and Mathematics, Universidad del Rosario, Carrera 24, No. 63C-69, Bogotá D.C. 111221, Colombia.

15. Laboratoire Ecologie, Evolution, Interactions des Systèmes Amazoniens (LEEISA), USR 3456, Université De Guyane, CNRS Guyane, 275 Route de Montabo, 97334 Cayenne, French Guiana.

16. Department of Biological Sciences, Mississippi State University, Starkville, MS 39762, USA.

17. Molecular Sciences and Research Center, University of Puerto Rico, San Juan, PR 00931-3360, Puerto Rico.

18. Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853, USA.

19. Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637, USA.

20. CEFE, CNRS, Université de Montpellier, Université Paul Valéry Montpellier 3, EPHE, IRD, 34090 Montpellier, France.

21. Smithsonian Tropical Research Institute, Apartado 0843-03092 Panamá, Panama.

22. Department of Mathematics, University of Texas, Austin, TX 78712, USA.

23. 10x Genomics, Pleasanton, CA 94566, USA.

Abstract

We used 20 de novo genome assemblies to probe the speciation history and architecture of gene flow in rapidly radiating Heliconius butterflies. Our tests to distinguish incomplete lineage sorting from introgression indicate that gene flow has obscured several ancient phylogenetic relationships in this group over large swathes of the genome. Introgressed loci are underrepresented in low-recombination and gene-rich regions, consistent with the purging of foreign alleles more tightly linked to incompatibility loci. Here, we identify a hitherto unknown inversion that traps a color pattern switch locus. We infer that this inversion was transferred between lineages by introgression and is convergent with a similar rearrangement in another part of the genus. These multiple de novo genome sequences enable improved understanding of the importance of introgression and selective processes in adaptive radiation.

Funder

National Science Foundation

National Institutes of Health

Biotechnology and Biological Sciences Research Council

Air Force Office of Scientific Research

Natural Environment Research Council

European Commission

Natural Sciences and Engineering Research Council of Canada

Broad Institute

Smithsonian Tropical Research Institute

University of Cambridge

Universidad del Rosario

Agence Nationale de la Recherche

Conselho Nacional de Desenvolvimento Científico e Tecnológico

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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