Targeted Capture of Hundreds of Nuclear Genes Unravels Phylogenetic Relationships of the Diverse Neotropical Palm Tribe Geonomateae
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Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2019 Targeted capture of hundreds of nuclear genes unravels phylogenetic relationships of the diverse neotropical palm tribe Geonomateae Loiseau, Oriane ; Olivares, Ingrid ; Paris, Margot ; de La Harpe, Marylaure ; Weigand, Anna ; Koubínová, Darina ; Rolland, Jonathan ; Bacon, Christine D ; Balslev, Henrik ; Borchsenius, Finn ; Cano, Angela ; Couvreur, Thomas L P ; Delnatte, César ; Fardin, Frédérique ; Gayot, Marc ; Mejía, Fabian ; Mota-Machado, Talita ; Perret, Mathieu ; Roncal, Julissa ; Sanin, Maria José ; Stauffer, Fred ; Lexer, Christian ; Kessler, Michael ; Salamin, Nicolas DOI: https://doi.org/10.3389/fpls.2019.00864 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-172087 Journal Article Published Version The following work is licensed under a Creative Commons: Attribution 4.0 International (CC BY 4.0) License. Originally published at: Loiseau, Oriane; Olivares, Ingrid; Paris, Margot; de La Harpe, Marylaure; Weigand, Anna; Koubínová, Darina; Rolland, Jonathan; Bacon, Christine D; Balslev, Henrik; Borchsenius, Finn; Cano, Angela; Couvreur, Thomas L P; Delnatte, César; Fardin, Frédérique; Gayot, Marc; Mejía, Fabian; Mota-Machado, Talita; Perret, Mathieu; Roncal, Julissa; Sanin, Maria José; Stauffer, Fred; Lexer, Christian; Kessler, Michael; Salamin, Nicolas (2019). Targeted capture of hundreds of nuclear genes unravels phylogenetic relationships of the diverse neotropical palm tribe Geonomateae. Frontiers in Plant Science, 10:864. DOI: https://doi.org/10.3389/fpls.2019.00864 fpls-10-00864 July 12, 2019 Time: 16:6 # 1 ORIGINAL RESEARCH published: 12 July 2019 doi: 10.3389/fpls.2019.00864 Targeted Capture of Hundreds of Nuclear Genes Unravels Phylogenetic Relationships of the Diverse Neotropical Palm Tribe Geonomateae Oriane Loiseau1, Ingrid Olivares2,3, Margot Paris4, Marylaure de La Harpe5, Edited by: Anna Weigand2, Darina Koubínová1,6, Jonathan Rolland1,7, Christine D. Bacon8,9, Lisa Pokorny, Henrik Balslev10, Finn Borchsenius11, Angela Cano12, Thomas L. P. Couvreur13, Instituto Nacional de Investigación y César Delnatte14, Frédérique Fardin15, Marc Gayot16, Fabian Mejía17, Tecnología Agraria y Alimentaria, Talita Mota-Machado18, Mathieu Perret19, Julissa Roncal20, Maria José Sanin17, Spain Fred Stauffer19, Christian Lexer5, Michael Kessler2† and Nicolas Salamin1*† Reviewed by: Karolina Heyduk, 1 Department of Computational Biology, University of Lausanne, Lausanne, Switzerland, 2 Department for Systematic Yale University, United States and Evolutionary Botany, University of Zurich, Zurich, Switzerland, 3 Centre for Biodiversity and Environment Research, Zhen Li, University College London, London, United Kingdom, 4 Department of Biology, Unit Ecology and Evolution, University Ghent University, Belgium of Fribourg, Fribourg, Switzerland, 5 Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria, 6 7 *Correspondence: Natural History Museum of Geneva, Geneva, Switzerland, Department of Zoology, University of British Columbia, 8 Nicolas Salamin Vancouver, BC, Canada, Department of Biological and Environmental Sciences, University of Gothenburg, Gothenburg, 9 10 [email protected] Sweden, Gothenburg Global Biodiversity Centre, Gothenburg, Sweden, Department of Bioscience, Biodiversity and Ecoinformatics, Aarhus University, Aarhus, Denmark, 11 Science Museums, Aarhus University, Aarhus, Denmark, † Share co-last authorship 12 Cambridge University Botanic Garden, Cambridge, United Kingdom, 13 IRD, DIADE, University of Montpellier, Montpellier, France, 14 National Forestry Office, Fort-de-France, France, 15 Parc National de la Guadeloupe, Guadeloupe, France, Specialty section: 16 National Forestry Office, Guadeloupe, France, 17 Facultad de Ciencias y Biotecnología, Universidad CES, Medellin, This article was submitted to Colombia, 18 Programa de Pós-Graduação em Biologia Vegetal, Departamento de Botânica, Instituto de Ciências Biológicas, Plant Systematics and Evolution, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil, 19 Department of Botany and Plant Biology, Conservatory a section of the journal and Botanical Garden of the City of Geneva, University of Geneva, Geneva, Switzerland, 20 Department of Biology, Memorial Frontiers in Plant Science University of Newfoundland, St. John’s, NL, Canada Received: 14 January 2019 Accepted: 17 June 2019 The tribe Geonomateae is a widely distributed group of 103 species of Neotropical Published: 12 July 2019 palms which contains six ecologically important understory or subcanopy genera. Citation: Loiseau O, Olivares I, Paris M, Although it has been the focus of many studies, our understanding of the evolutionary de La Harpe M, Weigand A, history of this group, and in particular of the taxonomically complex genus Geonoma, Koubínová D, Rolland J, Bacon CD, Balslev H, Borchsenius F, Cano A, is far from complete due to a lack of molecular data. Specifically, the previous Sanger Couvreur TLP, Delnatte C, Fardin F, sequencing-based studies used a few informative characters and partial sampling. To Gayot M, Mejía F, Mota-Machado T, overcome these limitations, we used a recently developed Arecaceae-specific target Perret M, Roncal J, Sanin MJ, Stauffer F, Lexer C, Kessler M and capture bait set to undertake a phylogenomic analysis of the tribe Geonomateae. Salamin N (2019) Targeted Capture We sequenced 3,988 genomic regions for 85% of the species of the tribe, including of Hundreds of Nuclear Genes Unravels Phylogenetic Relationships 84% of the species of the largest genus, Geonoma. Phylogenetic relationships were of the Diverse Neotropical Palm Tribe inferred using both concatenation and coalescent methods. Overall, our phylogenetic Geonomateae. tree is highly supported and congruent with taxonomic delimitations although several Front. Plant Sci. 10:864. doi: 10.3389/fpls.2019.00864 morphological taxa were revealed to be non-monophyletic. It is the first time that such Frontiers in Plant Science| www.frontiersin.org 1 July 2019| Volume 10| Article 864 fpls-10-00864 July 12, 2019 Time: 16:6 # 2 Loiseau et al. Phylogenomics of Neotropical Geonomateae Palms a large genomic dataset is provided for an entire tribe within the Arecaceae. Our study lays the groundwork not only for detailed macro- and micro-evolutionary studies within the group, but also sets a workflow for understanding other species complexes across the tree of life. Keywords: Arecaceae, Geonoma, Neotropics, phylogenetic informativeness, phylogenomics, species complexes INTRODUCTION some extent. Considerable research has also been dedicated to investigate the phenotypically widely variable species complexes Palms (Arecaceae) are an important ecological component that represent 20% of the species of Geonoma (Borchsenius, (Henderson, 2002; Couvreur et al., 2011) and a useful plant 2002; Henderson and Martins, 2002; Roncal, 2006; Roncal group of tropical ecosystems (Macia et al., 2011; Gruca et al., et al., 2007; Henderson, 2011; Borchsenius et al., 2016). 2015). The palm family was recently advocated as a model Despite all these efforts, the evolutionary history of Geonoma group to understand the evolution of tropical rain forests and Geonomateae remains only partially understood due to (Baker and Couvreur, 2013) and numerous studies have the paucity of DNA sequences, which so far are available investigated their phylogenetic relationships and systematics only for three nuclear loci and approximately 60% of the (Uhl and Dransfield, 1987; Baker et al., 1999; Dransfield species in the tribe. et al., 2008; Baker and Dransfield, 2016). However, given Obtaining a robust phylogenetic hypothesis for the the remarkably low rate of molecular evolution observed in Geonomateae is therefore crucial to enable a reliable assessment palms (Wilson et al., 1990), phylogenetic studies at different of the systematic relationships of its lineages, but also to taxonomic levels within the Arecaceae based on a few provide the foundation to assess the macroevolutionary plastid or nuclear genes generally result in poorly resolved patterns and the dynamics of diversification in this key phylogenetic trees, especially at the species level (Roncal palm group. The increasing affordability of next generation et al., 2005, 2008; Cuenca et al., 2008; Baker et al., 2011; sequencing techniques, which offers the possibility to sequence Bacon et al., 2012a, 2016a,b, 2017; Meerow et al., 2015; hundreds of loci at a time, has already benefitted many Sanín et al., 2016). plant phylogenetic studies (e.g., Nicholls et al., 2015; Sass The lack of informative genetic markers, combined et al., 2016; Mandel et al., 2017; Mitchell et al., 2017). For with insufficient taxonomic sampling, currently limits our Arecaceae, while most of genome-scale data initially focused understanding of the phylogenetic relationships within the on commercially important species such as the oil palm most diverse palm genera in the Neotropics, such as Bactris (Uthaipaisanwong et al., 2012; Singh et al., 2013) and the Jacq. ex Scop., Chamaedorea Willd., and Geonoma Willd. These date palm (Yang et al., 2010; Al-Mssallem et al., 2013), three genera are mostly small shade-adapted palms and they evolutionary biologists have put considerable effort in the contain the most abundant palm species in the understory last few years to generate genomic data across the whole of many Neotropical forests