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Highly differentiated loci resolve phylogenetic relationships in the Bean Goose complex

BACKGROUND: Reconstructing phylogenetic relationships with genomic data remains a challenging endeavor. Numerous phylogenomic studies have reported incongruent gene trees when analyzing different genomic regions, complicating the search for a ‘true’ species tree. Some authors have argued that genomi...

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Autores principales: Ottenburghs, Jente, Honka, Johanna, Heikkinen, Marja E., Madsen, Jesper, Müskens, Gerhard J. D. M., Ellegren, Hans
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9854053/
https://www.ncbi.nlm.nih.gov/pubmed/36658479
http://dx.doi.org/10.1186/s12862-023-02103-3
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author Ottenburghs, Jente
Honka, Johanna
Heikkinen, Marja E.
Madsen, Jesper
Müskens, Gerhard J. D. M.
Ellegren, Hans
author_facet Ottenburghs, Jente
Honka, Johanna
Heikkinen, Marja E.
Madsen, Jesper
Müskens, Gerhard J. D. M.
Ellegren, Hans
author_sort Ottenburghs, Jente
collection PubMed
description BACKGROUND: Reconstructing phylogenetic relationships with genomic data remains a challenging endeavor. Numerous phylogenomic studies have reported incongruent gene trees when analyzing different genomic regions, complicating the search for a ‘true’ species tree. Some authors have argued that genomic regions of increased divergence (i.e. differentiation islands) reflect the species tree, although other studies have shown that these regions might produce misleading topologies due to species-specific selective sweeps or ancient introgression events. In this study, we tested the extent to which highly differentiated loci can resolve phylogenetic relationships in the Bean Goose complex, a group of goose taxa that includes the Taiga Bean Goose (Anser fabalis), the Tundra Bean Goose (Anser serrirostris) and the Pink-footed Goose (Anser brachyrhynchus). RESULTS: First, we show that a random selection of genomic loci—which mainly samples the undifferentiated regions of the genome—results in an unresolved species complex with a monophyletic A. brachyrhynchus embedded within a paraphyletic cluster of A. fabalis and A. serrirostris. Next, phylogenetic analyses of differentiation islands converged upon a topology of three monophyletic clades in which A. brachyrhynchus is sister to A. fabalis, and A. serrirostris is sister to the clade uniting these two species. Close inspection of the locus trees within the differentiated regions revealed that this topology was consistently supported over other phylogenetic arrangements. As it seems unlikely that selection or introgression events have impacted all differentiation islands in the same way, we are convinced that this topology reflects the ‘true’ species tree. Additional analyses, based on D-statistics, revealed extensive introgression between A. fabalis and A. serrirostris, which partly explains the failure to resolve the species complex with a random selection of genomic loci. Recent introgression between these taxa has probably erased the phylogenetic branching pattern across a large section of the genome, whereas differentiation islands were unaffected by the homogenizing gene flow and maintained the phylogenetic patterns that reflect the species tree. CONCLUSIONS: The evolution of the Bean Goose complex can be depicted as a simple bifurcating tree, but this would ignore the impact of introgressive hybridization. Hence, we advocate that the evolutionary relationships between these taxa are best represented as a phylogenetic network. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-023-02103-3.
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spelling pubmed-98540532023-01-21 Highly differentiated loci resolve phylogenetic relationships in the Bean Goose complex Ottenburghs, Jente Honka, Johanna Heikkinen, Marja E. Madsen, Jesper Müskens, Gerhard J. D. M. Ellegren, Hans BMC Ecol Evol Research BACKGROUND: Reconstructing phylogenetic relationships with genomic data remains a challenging endeavor. Numerous phylogenomic studies have reported incongruent gene trees when analyzing different genomic regions, complicating the search for a ‘true’ species tree. Some authors have argued that genomic regions of increased divergence (i.e. differentiation islands) reflect the species tree, although other studies have shown that these regions might produce misleading topologies due to species-specific selective sweeps or ancient introgression events. In this study, we tested the extent to which highly differentiated loci can resolve phylogenetic relationships in the Bean Goose complex, a group of goose taxa that includes the Taiga Bean Goose (Anser fabalis), the Tundra Bean Goose (Anser serrirostris) and the Pink-footed Goose (Anser brachyrhynchus). RESULTS: First, we show that a random selection of genomic loci—which mainly samples the undifferentiated regions of the genome—results in an unresolved species complex with a monophyletic A. brachyrhynchus embedded within a paraphyletic cluster of A. fabalis and A. serrirostris. Next, phylogenetic analyses of differentiation islands converged upon a topology of three monophyletic clades in which A. brachyrhynchus is sister to A. fabalis, and A. serrirostris is sister to the clade uniting these two species. Close inspection of the locus trees within the differentiated regions revealed that this topology was consistently supported over other phylogenetic arrangements. As it seems unlikely that selection or introgression events have impacted all differentiation islands in the same way, we are convinced that this topology reflects the ‘true’ species tree. Additional analyses, based on D-statistics, revealed extensive introgression between A. fabalis and A. serrirostris, which partly explains the failure to resolve the species complex with a random selection of genomic loci. Recent introgression between these taxa has probably erased the phylogenetic branching pattern across a large section of the genome, whereas differentiation islands were unaffected by the homogenizing gene flow and maintained the phylogenetic patterns that reflect the species tree. CONCLUSIONS: The evolution of the Bean Goose complex can be depicted as a simple bifurcating tree, but this would ignore the impact of introgressive hybridization. Hence, we advocate that the evolutionary relationships between these taxa are best represented as a phylogenetic network. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-023-02103-3. BioMed Central 2023-01-19 /pmc/articles/PMC9854053/ /pubmed/36658479 http://dx.doi.org/10.1186/s12862-023-02103-3 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Ottenburghs, Jente
Honka, Johanna
Heikkinen, Marja E.
Madsen, Jesper
Müskens, Gerhard J. D. M.
Ellegren, Hans
Highly differentiated loci resolve phylogenetic relationships in the Bean Goose complex
title Highly differentiated loci resolve phylogenetic relationships in the Bean Goose complex
title_full Highly differentiated loci resolve phylogenetic relationships in the Bean Goose complex
title_fullStr Highly differentiated loci resolve phylogenetic relationships in the Bean Goose complex
title_full_unstemmed Highly differentiated loci resolve phylogenetic relationships in the Bean Goose complex
title_short Highly differentiated loci resolve phylogenetic relationships in the Bean Goose complex
title_sort highly differentiated loci resolve phylogenetic relationships in the bean goose complex
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9854053/
https://www.ncbi.nlm.nih.gov/pubmed/36658479
http://dx.doi.org/10.1186/s12862-023-02103-3
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