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

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; Hiscock, Simon J

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. [Abstract copyright: Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.]

Citation

Nevado, B., Chapman, M. A., Brennan, A. C., Clark, J. W., Wong, E. L. Y., Batstone, T., McCarthy, S. A., Tracey, A., Torrance, J., Sims, Y., Abbott, R. J., Filatov, D., & Hiscock, S. J. (2024). Genomic changes and stabilization following homoploid hybrid speciation of the Oxford ragwort Senecio squalidus. Current Biology, 34(19), 4412-4423.e5. https://doi.org/10.1016/j.cub.2024.08.009

• Journal Article Type: Article
• Acceptance Date: Aug 7, 2024
• Online Publication Date: Sep 5, 2024
• Publication Date: Oct 7, 2024
• Deposit Date: Oct 2, 2024
• Publicly Available Date: Oct 3, 2024
• Journal: Current biology : CB
• Print ISSN: 0960-9822
• Electronic ISSN: 1879-0445
• Publisher: Cell Press
• Peer Reviewed: Peer Reviewed
• Volume: 34
• Issue: 19
• Pages: 4412-4423.e5
• DOI: https://doi.org/10.1016/j.cub.2024.08.009
• Keywords: genome assembly, Oxford ragwort, linkage disequilibrium, population genomics, natural selection, genetic incompatibilities, Senecio squalidus, RNA-seq, homoploid hybrid speciation
• Public URL: https://durham-repository.worktribe.com/output/2892918