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The role of geography, ecology, and hybridization in the evolutionary history of Canary Island Descurainia

The role of geography, ecology, and hybridization in the evolutionary history of Canary Island Descurainia
The role of geography, ecology, and hybridization in the evolutionary history of Canary Island Descurainia
Premise: oceanic islands offer the opportunity to understand evolutionary processes underlying rapid diversification. Along with geographic isolation and ecological shifts, a growing body of genomic evidence has suggested that hybridization can play an important role in island evolution. Here we use genotyping-by-sequencing (GBS) to understand the roles of hybridization, ecology, and geographic isolation in the radiation of Canary Island Descurainia (Brassicaceae).

Methods: we carried out GBS for multiple individuals of all Canary Island species and two outgroups. Phylogenetic analyses of the GBS data were performed using both supermatrix and gene tree approaches and hybridization events were examined using D-statistics and Approximate Bayesian Computation. Climatic data were analyzed to examine the relationship between ecology and diversification.

Results: analysis of the supermatrix data set resulted in a fully resolved phylogeny. Species networks suggest a hybridization event has occurred for D. gilva, with these results being supported by Approximate Bayesian Computation analysis. Strong phylogenetic signals for temperature and precipitation indicate one major ecological shift within Canary Island Descurainia.

Conclusions: inter-island dispersal played a significant role in the diversification of Descurainia, with evidence of only one major shift in climate preferences. Despite weak reproductive barriers and the occurrence of hybrids, hybridization appears to have played only a limited role in the diversification of the group with a single instance detected. The results highlight the need to use phylogenetic network approaches that can simultaneously accommodate incomplete lineage sorting and gene flow when studying groups prone to hybridization; patterns that might otherwise be obscured in species trees.
ABBA-BABA, Descurainia, biogeography, diversification, genotyping-by-sequencing (GBS), hybridization, phylogenetics, speciation, species networks
0002-9122
Jackson, Amy
732a7afe-b36d-421f-a6ba-624e4bc801b7
White, Oliver William
c049ec63-de89-4360-a3a1-ae1b13fa82d2
Carine, Mark A.
eeaed5aa-bc4b-43ec-a667-b6c45e3217ed
Chapman, Mark
8bac4a92-bfa7-4c3c-af29-9af852ef6383
Jackson, Amy
732a7afe-b36d-421f-a6ba-624e4bc801b7
White, Oliver William
c049ec63-de89-4360-a3a1-ae1b13fa82d2
Carine, Mark A.
eeaed5aa-bc4b-43ec-a667-b6c45e3217ed
Chapman, Mark
8bac4a92-bfa7-4c3c-af29-9af852ef6383

Jackson, Amy, White, Oliver William, Carine, Mark A. and Chapman, Mark (2023) The role of geography, ecology, and hybridization in the evolutionary history of Canary Island Descurainia. American Journal of Botany, 110 (5), [e16162]. (doi:10.1002/ajb2.16162).

Record type: Article

Abstract

Premise: oceanic islands offer the opportunity to understand evolutionary processes underlying rapid diversification. Along with geographic isolation and ecological shifts, a growing body of genomic evidence has suggested that hybridization can play an important role in island evolution. Here we use genotyping-by-sequencing (GBS) to understand the roles of hybridization, ecology, and geographic isolation in the radiation of Canary Island Descurainia (Brassicaceae).

Methods: we carried out GBS for multiple individuals of all Canary Island species and two outgroups. Phylogenetic analyses of the GBS data were performed using both supermatrix and gene tree approaches and hybridization events were examined using D-statistics and Approximate Bayesian Computation. Climatic data were analyzed to examine the relationship between ecology and diversification.

Results: analysis of the supermatrix data set resulted in a fully resolved phylogeny. Species networks suggest a hybridization event has occurred for D. gilva, with these results being supported by Approximate Bayesian Computation analysis. Strong phylogenetic signals for temperature and precipitation indicate one major ecological shift within Canary Island Descurainia.

Conclusions: inter-island dispersal played a significant role in the diversification of Descurainia, with evidence of only one major shift in climate preferences. Despite weak reproductive barriers and the occurrence of hybrids, hybridization appears to have played only a limited role in the diversification of the group with a single instance detected. The results highlight the need to use phylogenetic network approaches that can simultaneously accommodate incomplete lineage sorting and gene flow when studying groups prone to hybridization; patterns that might otherwise be obscured in species trees.

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Accepted/In Press date: 15 March 2023
e-pub ahead of print date: 29 May 2023
Published date: May 2023
Additional Information: Funding Information: The authors would like to thank Rachael Graham and Alfredo Reyes‐Bentacourt for Canary Island field sampling. We also thank Barbara Goodson and Bob Jansen (University of Texas) for providing DNA samples, and the Banco de Germoplasma Vegetal (BGV) Seedbank for providing seeds. We are grateful to the following national parks for permits to collect. Cabildo de Tenerife (permit no. 22835), Parque Nacional del Teide (permit no. 24339), Cabildo de La Palma (permit no. 2016005709), Parque Nacional de la Caldera de Taburiente (permit no. 671303), Parque Nacional Garajonay (permit no. 25771), Cabildo de Gran Canaria (permit no. 16267), and Gobierno de Canarias (permit no. 671303). We would like to thank the reviewers for their helpful and insightful comments, which helped improve our manuscript. This work was supported by a Ph.D. studentship to ACJ from the Natural Environmental Research Council (grant number NE/L002531/1). We acknowledge the use of the IRIDIS High Performance Computing Facility, and associated support services at the University of Southampton, in the completion of this work. Descurainia Funding Information: The authors would like to thank Rachael Graham and Alfredo Reyes-Bentacourt for Canary Island field sampling. We also thank Barbara Goodson and Bob Jansen (University of Texas) for providing DNA samples, and the Banco de Germoplasma Vegetal (BGV) Seedbank for providing Descurainia seeds. We are grateful to the following national parks for permits to collect. Cabildo de Tenerife (permit no. 22835), Parque Nacional del Teide (permit no. 24339), Cabildo de La Palma (permit no. 2016005709), Parque Nacional de la Caldera de Taburiente (permit no. 671303), Parque Nacional Garajonay (permit no. 25771), Cabildo de Gran Canaria (permit no. 16267), and Gobierno de Canarias (permit no. 671303). We would like to thank the reviewers for their helpful and insightful comments, which helped improve our manuscript. This work was supported by a Ph.D. studentship to ACJ from the Natural Environmental Research Council (grant number NE/L002531/1). We acknowledge the use of the IRIDIS High Performance Computing Facility, and associated support services at the University of Southampton, in the completion of this work. Publisher Copyright: © 2023 The Authors. American Journal of Botany published by Wiley Periodicals LLC on behalf of Botanical Society of America.
Keywords: ABBA-BABA, Descurainia, biogeography, diversification, genotyping-by-sequencing (GBS), hybridization, phylogenetics, speciation, species networks

Identifiers

Local EPrints ID: 477738
URI: http://eprints.soton.ac.uk/id/eprint/477738
ISSN: 0002-9122
PURE UUID: 7a3b96dd-2251-4d08-986c-d71438316343
ORCID for Amy Jackson: ORCID iD orcid.org/0000-0003-0660-0181
ORCID for Mark Chapman: ORCID iD orcid.org/0000-0002-7151-723X

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Date deposited: 13 Jun 2023 17:27
Last modified: 18 Mar 2024 03:49

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Contributors

Author: Amy Jackson ORCID iD
Author: Oliver William White
Author: Mark A. Carine
Author: Mark Chapman ORCID iD

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