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Genomic changes and stabilization following homoploid hybrid speciation of the Oxford ragwort Senecio squalidus

Genomic changes and stabilization following homoploid hybrid speciation of the Oxford ragwort Senecio squalidus
Genomic changes and stabilization following homoploid hybrid speciation of the Oxford ragwort Senecio squalidus

Oxford ragwort (Senecio squalidus) is one of only two homoploid hybrid species known to have originated very recently, so it is a unique model for determining genomic changes and stabilization following homoploid hybrid speciation. Here, we provide a chromosome-level genome assembly of S. squalidus with 95% of the assembly contained in the 10 longest scaffolds, corresponding to its haploid chromosome number. We annotated 30,249 protein-coding genes and estimated that ∼62% of the genome consists of repetitive elements. We then characterized genome-wide patterns of linkage disequilibrium, polymorphism, and divergence in S. squalidus and its two parental species, finding that (1) linkage disequilibrium is highly heterogeneous, with a region on chromosome 4 showing increased values across all three species but especially in S. squalidus; (2) regions harboring genetic incompatibilities between the two parental species tend to be large, show reduced recombination, and have lower polymorphism in S. squalidus; (3) the two parental species have an unequal contribution (70:30) to the genome of S. squalidus, with long blocks of parent-specific ancestry supporting a very rapid stabilization of the hybrid lineage after hybrid formation; and (4) genomic regions with major parent ancestry exhibit an overrepresentation of loci with evidence for divergent selection occurring between the two parental species on Mount Etna. Our results show that both genetic incompatibilities and natural selection play a role in determining genome-wide reorganization following hybrid speciation and that patterns associated with homoploid hybrid speciation-typically seen in much older systems-can evolve very quickly following hybridization.

Genetic Speciation, Genome, Plant, Hybridization, Genetic, Linkage Disequilibrium, Senecio/genetics
0960-9822
4412-4423
Nevado, Bruno
d3d265c6-dee2-4829-8d9c-7cede02575b8
Chapman, Mark A.
8bac4a92-bfa7-4c3c-af29-9af852ef6383
Brennan, Adrian C.
5e7889da-d72d-41ca-a232-87823eaf4942
Clark, James W.
de70884d-445d-4b84-ab21-6e7657567e52
Wong, Edgar L.Y.
19f55dd1-0096-4131-996e-c75a971ca14f
Batstone, Tom
70132df8-eb4f-46f3-845c-94e1e9a49e68
McCarthy, Shane A.
a380714a-9c12-4d60-98eb-e89583738480
Tracey, Alan
592ddb2c-c868-41c8-970f-7371d14e7272
Torrance, James
d88001e4-5722-4494-b9a8-da7ef5a88ff1
Sims, Ying
ea18c14f-a1bb-4344-88f2-7fad0678db8a
Abbott, Richard J.
d52f6834-ba40-4c9f-9aa5-9be0b4184b6b
Filatov, Dmitry
6915d6cb-16dd-44dd-b12e-e9a91b5dd199
Hiscock, Simon J.
74e2b6d9-77a8-46ce-9d00-dfb326d34433
Nevado, Bruno
d3d265c6-dee2-4829-8d9c-7cede02575b8
Chapman, Mark A.
8bac4a92-bfa7-4c3c-af29-9af852ef6383
Brennan, Adrian C.
5e7889da-d72d-41ca-a232-87823eaf4942
Clark, James W.
de70884d-445d-4b84-ab21-6e7657567e52
Wong, Edgar L.Y.
19f55dd1-0096-4131-996e-c75a971ca14f
Batstone, Tom
70132df8-eb4f-46f3-845c-94e1e9a49e68
McCarthy, Shane A.
a380714a-9c12-4d60-98eb-e89583738480
Tracey, Alan
592ddb2c-c868-41c8-970f-7371d14e7272
Torrance, James
d88001e4-5722-4494-b9a8-da7ef5a88ff1
Sims, Ying
ea18c14f-a1bb-4344-88f2-7fad0678db8a
Abbott, Richard J.
d52f6834-ba40-4c9f-9aa5-9be0b4184b6b
Filatov, Dmitry
6915d6cb-16dd-44dd-b12e-e9a91b5dd199
Hiscock, Simon J.
74e2b6d9-77a8-46ce-9d00-dfb326d34433

Nevado, Bruno, Chapman, Mark A., Brennan, Adrian C., Clark, James W., Wong, Edgar L.Y., Batstone, Tom, McCarthy, Shane A., Tracey, Alan, Torrance, James, Sims, Ying, Abbott, Richard J., Filatov, Dmitry and Hiscock, Simon J. (2024) Genomic changes and stabilization following homoploid hybrid speciation of the Oxford ragwort Senecio squalidus. Current biology : CB, 34 (19), 4412-4423, [e5]. (doi:10.1016/j.cub.2024.08.009).

Record type: Article

Abstract

Oxford ragwort (Senecio squalidus) is one of only two homoploid hybrid species known to have originated very recently, so it is a unique model for determining genomic changes and stabilization following homoploid hybrid speciation. Here, we provide a chromosome-level genome assembly of S. squalidus with 95% of the assembly contained in the 10 longest scaffolds, corresponding to its haploid chromosome number. We annotated 30,249 protein-coding genes and estimated that ∼62% of the genome consists of repetitive elements. We then characterized genome-wide patterns of linkage disequilibrium, polymorphism, and divergence in S. squalidus and its two parental species, finding that (1) linkage disequilibrium is highly heterogeneous, with a region on chromosome 4 showing increased values across all three species but especially in S. squalidus; (2) regions harboring genetic incompatibilities between the two parental species tend to be large, show reduced recombination, and have lower polymorphism in S. squalidus; (3) the two parental species have an unequal contribution (70:30) to the genome of S. squalidus, with long blocks of parent-specific ancestry supporting a very rapid stabilization of the hybrid lineage after hybrid formation; and (4) genomic regions with major parent ancestry exhibit an overrepresentation of loci with evidence for divergent selection occurring between the two parental species on Mount Etna. Our results show that both genetic incompatibilities and natural selection play a role in determining genome-wide reorganization following hybrid speciation and that patterns associated with homoploid hybrid speciation-typically seen in much older systems-can evolve very quickly following hybridization.

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More information

Accepted/In Press date: 7 August 2024
e-pub ahead of print date: 10 September 2024
Published date: 7 October 2024
Keywords: Genetic Speciation, Genome, Plant, Hybridization, Genetic, Linkage Disequilibrium, Senecio/genetics

Identifiers

Local EPrints ID: 494686
URI: http://eprints.soton.ac.uk/id/eprint/494686
ISSN: 0960-9822
PURE UUID: a5946ab1-e3e8-4880-99a8-c21d8ec1956f
ORCID for Mark A. Chapman: ORCID iD orcid.org/0000-0002-7151-723X

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Date deposited: 14 Oct 2024 16:38
Last modified: 19 Oct 2024 01:46

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Contributors

Author: Bruno Nevado
Author: Mark A. Chapman ORCID iD
Author: Adrian C. Brennan
Author: James W. Clark
Author: Edgar L.Y. Wong
Author: Tom Batstone
Author: Shane A. McCarthy
Author: Alan Tracey
Author: James Torrance
Author: Ying Sims
Author: Richard J. Abbott
Author: Dmitry Filatov
Author: Simon J. Hiscock

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