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Hybrid speciation driven by multilocus introgression of ecological traits

Rosser, Neil ; Seixas, Fernando ; Queste, Lucie M. ; Cama, Bruna ; Mori-Pezo, Ronald ; Kryvokhyzha, Dmytro LU ; Nelson, Michaela ; Waite-Hudson, Rachel ; Goringe, Matt and Costa, Mauro , et al. (2024) In Nature 628. p.811-817
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... (More)

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.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
in
Nature
volume
628
pages
811 - 817
publisher
Nature Publishing Group
external identifiers
  • pmid:38632397
  • scopus:85190684635
ISSN
0028-0836
DOI
10.1038/s41586-024-07263-w
language
English
LU publication?
yes
additional info
Publisher Copyright: © The Author(s) 2024.
id
d5c55d78-6d46-43e5-b158-33bd62167bfe
date added to LUP
2024-04-29 11:24:56
date last changed
2024-05-13 12:43:41
@article{d5c55d78-6d46-43e5-b158-33bd62167bfe,
  abstract     = {{<p>Hybridization allows adaptations to be shared among lineages and may trigger the evolution of new species<sup>1,2</sup>. However, convincing examples of homoploid hybrid speciation remain rare because it is challenging to demonstrate that hybridization was crucial in generating reproductive isolation<sup>3</sup>. 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.</p>}},
  author       = {{Rosser, Neil and Seixas, Fernando and Queste, Lucie M. and Cama, Bruna and Mori-Pezo, Ronald and Kryvokhyzha, Dmytro and Nelson, Michaela and Waite-Hudson, Rachel and Goringe, Matt and Costa, Mauro and Elias, Marianne and Mendes Eleres de Figueiredo, Clarisse and Freitas, André Victor Lucci and Joron, Mathieu and Kozak, Krzysztof and Lamas, Gerardo and Martins, Ananda R.P. and McMillan, W. Owen and Ready, Jonathan and Rueda-Muñoz, Nicol and Salazar, Camilo and Salazar, Patricio and Schulz, Stefan and Shirai, Leila T. and Silva-Brandão, Karina L. and Mallet, James and Dasmahapatra, Kanchon K.}},
  issn         = {{0028-0836}},
  language     = {{eng}},
  month        = {{04}},
  pages        = {{811--817}},
  publisher    = {{Nature Publishing Group}},
  series       = {{Nature}},
  title        = {{Hybrid speciation driven by multilocus introgression of ecological traits}},
  url          = {{http://dx.doi.org/10.1038/s41586-024-07263-w}},
  doi          = {{10.1038/s41586-024-07263-w}},
  volume       = {{628}},
  year         = {{2024}},
}