Hybrid speciation driven by multilocus introgression of ecological traits

Neil Rosser (), Fernando Seixas, Lucie M. Queste, Bruna Cama, Ronald Mori-Pezo, Dmytro Kryvokhyzha, Michaela Nelson, Rachel Waite-Hudson, Matt Goringe, Mauro Costa, Marianne Elias, Clarisse Mendes Eleres de Figueiredo, André Victor Lucci Freitas, Mathieu Joron, Krzysztof Kozak, Gerardo Lamas, Ananda R. P. Martins, W. Owen McMillan, Jonathan Ready, Nicol Rueda-Muñoz, Camilo Salazar, Patricio Salazar, Stefan Schulz, Leila T. Shirai, Karina L. Silva-Brandão, James Mallet () and Kanchon K. Dasmahapatra
Additional contact information
Neil Rosser: Harvard University
Fernando Seixas: Harvard University
Lucie M. Queste: University of York
Bruna Cama: University of York
Ronald Mori-Pezo: URKU Estudios Amazónicos
Dmytro Kryvokhyzha: Harvard University
Michaela Nelson: University of York
Rachel Waite-Hudson: University of York
Matt Goringe: University of York
Mauro Costa: Residencial Las Cumbres
Marianne Elias: Muséum National d’Histoire Naturelle
Clarisse Mendes Eleres de Figueiredo: Institute for Biological Sciences, Federal University of Pará (UFPA)
André Victor Lucci Freitas: Universidade Estadual de Campinas
Mathieu Joron: Université de Montpellier–Université Paul Valéry Montpellier–EPHE
Krzysztof Kozak: Smithsonian Tropical Research Institute
Gerardo Lamas: Universidad Nacional Mayor de San Marcos
Ananda R. P. Martins: McGill University
W. Owen McMillan: Smithsonian Tropical Research Institute
Jonathan Ready: Institute for Biological Sciences, Federal University of Pará (UFPA)
Nicol Rueda-Muñoz: Universidad del Rosario
Camilo Salazar: Universidad del Rosario
Patricio Salazar: University of Sheffield
Stefan Schulz: Institut für Organische Chemie, Technische Universität Braunschweig
Leila T. Shirai: Universidade Estadual de Campinas
Karina L. Silva-Brandão: Museum de Natur Hamburg Zoology
James Mallet: Harvard University
Kanchon K. Dasmahapatra: University of York

Nature, 2024, vol. 628, issue 8009, 811-817

Abstract: Abstract Hybridization allows adaptations to be shared among lineages and may trigger the evolution of new species1,2. However, convincing examples of homoploid hybrid speciation remain rare because it is challenging to demonstrate that hybridization was crucial in generating reproductive isolation3. Here we combine population genomic analysis with quantitative trait locus mapping of species-specific traits to examine a case of hybrid speciation in Heliconius butterflies. We show that Heliconius elevatus is a hybrid species that is sympatric with both parents and has persisted as an independently evolving lineage for at least 180,000 years. This is despite pervasive and ongoing gene flow with one parent, Heliconius pardalinus, which homogenizes 99% of their genomes. The remaining 1% introgressed from the other parent, Heliconius melpomene, and is scattered widely across the H. elevatus genome in islands of divergence from H. pardalinus. These islands contain multiple traits that are under disruptive selection, including colour pattern, wing shape, host plant preference, sex pheromones and mate choice. Collectively, these traits place H. elevatus on its own adaptive peak and permit coexistence with both parents. Our results show that speciation was driven by introgression of ecological traits, and that speciation with gene flow is possible with a multilocus genetic architecture.

Date: 2024
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DOI: 10.1038/s41586-024-07263-w

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