Comprehensive phylogenomic time tree of bryophytes reveals deep relationships and uncovers gene incongruences in the last 500 million years of diversification

Julia Bechteler^{1

2}, Gabriel Peñaloza-Bojacá³, David Bell⁴, J Gordon Burleigh⁵, Stuart F McDaniel⁵, E Christine Davis⁵, Emily B Sessa⁵, Alexander Bippus⁶, D Christine Cargill⁷, Sahut Chantanoarrapint⁸, Isabel Draper⁹, Lorena Endara⁵, Laura L Forrest⁴, Ricardo Garilleti¹⁰, Sean W Graham¹¹, Sanna Huttunen¹², Javier Jauregui Lazo¹³, Francisco Lara⁹, Juan Larraín¹⁴, Lily R Lewis⁵, David G Long⁴, Dietmar Quandt¹, Karen Renzaglia¹⁵, Alfons Schäfer-Verwimp¹⁶, Gaik Ee Lee¹⁷, Adriel M Sierra¹⁸, Matt von Konrat¹⁹, Charles E Zartman²⁰, Marta Regina Pereira²¹, Bernard Goffinet²², Juan Carlos Villarreal A¹⁸

Affiliations

¹ Nees-Institute for Plant Biodiversity, University of Bonn, Meckenheimer Allee 170, 53115, Bonn, Germany.
² Plant Biodiversity and Ecology, iES Landau, Institute for Environmental Sciences, RPTU University of Kaiserslautern-Landau, Fortstraße 7, 76829, Landau, Germany.
³ Laboratório de Sistemática Vegetal, Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Brazil.
⁴ Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH3 5LR, UK.
⁵ Department of Biological Sciences, University of Florida, 220 Bartram Hall, Gainesville, FL, 32611, USA.
⁶ California State Polytechnic University, Humboldt, Arcata, CA, 95521, USA.
⁷ Australian National Herbarium, Centre for Australian National Biodiversity Research, GPO Box 1700, Canberra, ACT, 2601, Australia.
⁸ PSU Herbarium, Division of Biological Science, Faculty of Science Prince of Songkla University, Hat Yai, Songkhla, 90110, Thailand.
⁹ Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, 28049 Madrid, Spain/Centro de Investigación en Biodiversidad y Cambio Global, Universidad Autónoma de Madrid, 28049, Madrid, Spain.
¹⁰ Departamento de Botánica y Geología. Universidad de Valencia, Avda. Vicente Andrés Estelles s/n, 46100, Burjassot, Spain.
¹¹ Department of Botany, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia, V6T 1Z4, Canada.
¹² Herbarium (TUR), Biodiversity Unit, 20014 University of Turku, Finland.
¹³ Department of Plant Biology and Genome Center, University of California Davis, 451 Health Sciences Drive, Davis, CA, 95616, USA.
¹⁴ Centro de Investigación en Recursos Naturales y Sustentabilidad (CIRENYS), Universidad Bernardo O'Higgins, Avenida Viel 1497, Santiago, Chile.
¹⁵ Department of Plant Biology, Southern Illinois University, Carbondale, IL, 62901, USA.
¹⁶ Mittlere Letten 11, 88634 Herdwangen-Schönach, Germany.
¹⁷ Faculty of Science and Marine Environment/Institute of Tropical Biodiversity and Sustainable Development, Universiti Malaysia Terengganu, 21020 Kuala Nerus, Terengganu, Malaysia.
¹⁸ Département de Biologie, Université Laval, Québec, Québec, G1V 0A6, Canada.
¹⁹ Gantz Family Collections Center, Field Museum, 1400 S. DuSable Lake Shore Drive, Chicago, IL, 60605, USA.
²⁰ Instituto Nacional de Pesquisas da Amazônia, Departamento de Biodiversidade, Avenida André Araújo, 2936, Aleixo, CEP 69060-001, Manaus, AM, Brazil.
²¹ Universidade do Estado do Amazonas, Av. Djalma Batista, 2470, Chapada, Manaus, 69050-010, Amazonas, Brazil.
²² Ecology and Evolutionary Biology, University of Connecticut, 75 North Eagleville Road, Storrs, CT, 06269-3043, USA.

PMID: 37792319
DOI: 10.1002/ajb2.16249

Free article

Comprehensive phylogenomic time tree of bryophytes reveals deep relationships and uncovers gene incongruences in the last 500 million years of diversification

Julia Bechteler et al. Am J Bot. 2023 Nov.

Free article

. 2023 Nov;110(11):e16249.

doi: 10.1002/ajb2.16249. Epub 2023 Nov 20.

Authors

Affiliations

¹ Nees-Institute for Plant Biodiversity, University of Bonn, Meckenheimer Allee 170, 53115, Bonn, Germany.
² Plant Biodiversity and Ecology, iES Landau, Institute for Environmental Sciences, RPTU University of Kaiserslautern-Landau, Fortstraße 7, 76829, Landau, Germany.
³ Laboratório de Sistemática Vegetal, Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Brazil.
⁴ Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH3 5LR, UK.
⁵ Department of Biological Sciences, University of Florida, 220 Bartram Hall, Gainesville, FL, 32611, USA.
⁶ California State Polytechnic University, Humboldt, Arcata, CA, 95521, USA.
⁷ Australian National Herbarium, Centre for Australian National Biodiversity Research, GPO Box 1700, Canberra, ACT, 2601, Australia.
⁸ PSU Herbarium, Division of Biological Science, Faculty of Science Prince of Songkla University, Hat Yai, Songkhla, 90110, Thailand.
⁹ Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, 28049 Madrid, Spain/Centro de Investigación en Biodiversidad y Cambio Global, Universidad Autónoma de Madrid, 28049, Madrid, Spain.
¹⁰ Departamento de Botánica y Geología. Universidad de Valencia, Avda. Vicente Andrés Estelles s/n, 46100, Burjassot, Spain.
¹¹ Department of Botany, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia, V6T 1Z4, Canada.
¹² Herbarium (TUR), Biodiversity Unit, 20014 University of Turku, Finland.
¹³ Department of Plant Biology and Genome Center, University of California Davis, 451 Health Sciences Drive, Davis, CA, 95616, USA.
¹⁴ Centro de Investigación en Recursos Naturales y Sustentabilidad (CIRENYS), Universidad Bernardo O'Higgins, Avenida Viel 1497, Santiago, Chile.
¹⁵ Department of Plant Biology, Southern Illinois University, Carbondale, IL, 62901, USA.
¹⁶ Mittlere Letten 11, 88634 Herdwangen-Schönach, Germany.
¹⁷ Faculty of Science and Marine Environment/Institute of Tropical Biodiversity and Sustainable Development, Universiti Malaysia Terengganu, 21020 Kuala Nerus, Terengganu, Malaysia.
¹⁸ Département de Biologie, Université Laval, Québec, Québec, G1V 0A6, Canada.
¹⁹ Gantz Family Collections Center, Field Museum, 1400 S. DuSable Lake Shore Drive, Chicago, IL, 60605, USA.
²⁰ Instituto Nacional de Pesquisas da Amazônia, Departamento de Biodiversidade, Avenida André Araújo, 2936, Aleixo, CEP 69060-001, Manaus, AM, Brazil.
²¹ Universidade do Estado do Amazonas, Av. Djalma Batista, 2470, Chapada, Manaus, 69050-010, Amazonas, Brazil.
²² Ecology and Evolutionary Biology, University of Connecticut, 75 North Eagleville Road, Storrs, CT, 06269-3043, USA.

PMID: 37792319
DOI: 10.1002/ajb2.16249

Abstract

Premise: Bryophytes form a major component of terrestrial plant biomass, structuring ecological communities in all biomes. Our understanding of the evolutionary history of hornworts, liverworts, and mosses has been significantly reshaped by inferences from molecular data, which have highlighted extensive homoplasy in various traits and repeated bursts of diversification. However, the timing of key events in the phylogeny, patterns, and processes of diversification across bryophytes remain unclear.

Methods: Using the GoFlag probe set, we sequenced 405 exons representing 228 nuclear genes for 531 species from 52 of the 54 orders of bryophytes. We inferred the species phylogeny from gene tree analyses using concatenated and coalescence approaches, assessed gene conflict, and estimated the timing of divergences based on 29 fossil calibrations.

Results: The phylogeny resolves many relationships across the bryophytes, enabling us to resurrect five liverwort orders and recognize three more and propose 10 new orders of mosses. Most orders originated in the Jurassic and diversified in the Cretaceous or later. The phylogenomic data also highlight topological conflict in parts of the tree, suggesting complex processes of diversification that cannot be adequately captured in a single gene-tree topology.

Conclusions: We sampled hundreds of loci across a broad phylogenetic spectrum spanning at least 450 Ma of evolution; these data resolved many of the critical nodes of the diversification of bryophytes. The data also highlight the need to explore the mechanisms underlying the phylogenetic ambiguity at specific nodes. The phylogenomic data provide an expandable framework toward reconstructing a comprehensive phylogeny of this important group of plants.

Keywords: Cretaceous diversification; hornworts; land plants; liverworts; mosses; phylogenetic discordance; rapid diversification; target capture.

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References

REFERENCES

1. Bechteler, J., G. Peñaloza-Bojacá, D. Bell, J. G. Burleigh, S. F. McDaniel, C. Davis, E. B. Sessa, et al. (2023). Comprehensive phylogenomic time tree of bryophytes reveals deep relationships and uncovers gene incongruences in the last 500 million years of diversification [Dataset]. Dryad. https://doi.org/10.5061/dryad.3j9kd51qm
1. Bell, D., Q. Lin, W. K. Gerelle, S. Joya, Y. Chang, Z. N. Taylor, C. J. Rothfels, et al. 2020. Organellomic data sets confirm a cryptic consensus on (unrooted) land-plant relationships and provide new insights into bryophyte molecular evolution. American Journal of Botany 107: 91-115.
1. Bell, N. E., D. Quandt, T. J. O'Brien, and A. E. Newton. 2007. Taxonomy and phylogeny in the earliest diverging pleurocarps: square holes and bifurcating pegs. Bryologist 110: 533-560.
1. Bennett, T., M. Liu, T. Aoyama, N. Bierfreund, M. Braun, Y. Coudert, R. Dennis, et al. 2014. Plasma membrane-targeted pin proteins drive shoot development in a moss. Current Biology 24: 2776-2785.
1. Benton, M. J., P. Wilf, and H. Sauquet. 2022. The Angiosperm Terrestrial Revolution and the origins of modern biodiversity. New Phytologist 233: 2017-2035.

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Comprehensive phylogenomic time tree of bryophytes reveals deep relationships and uncovers gene incongruences in the last 500 million years of diversification

Affiliations

Comprehensive phylogenomic time tree of bryophytes reveals deep relationships and uncovers gene incongruences in the last 500 million years of diversification

Authors

Affiliations

Abstract

References

REFERENCES

Publication types

MeSH terms

LinkOut - more resources

Full Text Sources