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Multigenic Phylogeny and Analysis of Tree Multigenic phylogeny and analysis of tree incongruences in Triticeae (Poaceae) Juan-Sebastian Escobar, Celine Scornavacca, Alberto Cenci, Claire Guilhaumon, Sylvain Santoni, Emmanuel Douzery, Vincent Ranwez, Sylvain Glémin, Jacques David To cite this version: Juan-Sebastian Escobar, Celine Scornavacca, Alberto Cenci, Claire Guilhaumon, Sylvain Santoni, et al.. Multigenic phylogeny and analysis of tree incongruences in Triticeae (Poaceae). BMC Evolutionary Biology, BioMed Central, 2011, 11 (181), 17 p. 10.1186/1471-2148-11-181. hal-01499047 HAL Id: hal-01499047 https://hal.archives-ouvertes.fr/hal-01499047 Submitted on 30 Mar 2017 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Escobar et al. BMC Evolutionary Biology 2011, 11:181 http://www.biomedcentral.com/1471-2148/11/181 RESEARCHARTICLE Open Access Multigenic phylogeny and analysis of tree incongruences in Triticeae (Poaceae) Juan S Escobar1,2,5*, Céline Scornavacca2,3,6, Alberto Cenci1,4,7, Claire Guilhaumon4, Sylvain Santoni4, Emmanuel JP Douzery2, Vincent Ranwez2, Sylvain Glémin2 and Jacques David4 Abstract Background: Introgressive events (e.g., hybridization, gene flow, horizontal gene transfer) and incomplete lineage sorting of ancestral polymorphisms are a challenge for phylogenetic analyses since different genes may exhibit conflicting genealogical histories. Grasses of the Triticeae tribe provide a particularly striking example of incongruence among gene trees. Previous phylogenies, mostly inferred with one gene, are in conflict for several taxon positions. Therefore, obtaining a resolved picture of relationships among genera and species of this tribe has been a challenging task. Here, we obtain the most comprehensive molecular dataset to date in Triticeae, including one chloroplastic and 26 nuclear genes. We aim to test whether it is possible to infer phylogenetic relationships in the face of (potentially) large-scale introgressive events and/or incomplete lineage sorting; to identify parts of the evolutionary history that have not evolved in a tree-like manner; and to decipher the biological causes of gene- tree conflicts in this tribe. Results: We obtain resolved phylogenetic hypotheses using the supermatrix and Bayesian Concordance Factors (BCF) approaches despite numerous incongruences among gene trees. These phylogenies suggest the existence of 4-5 major clades within Triticeae, with Psathyrostachys and Hordeum being the deepest genera. In addition, we construct a multigenic network that highlights parts of the Triticeae history that have not evolved in a tree-like manner. Dasypyrum, Heteranthelium and genera of clade V, grouping Secale, Taeniatherum, Triticum and Aegilops, have evolved in a reticulated manner. Their relationships are thus better represented by the multigenic network than by the supermatrix or BCF trees. Noteworthy, we demonstrate that gene-tree incongruences increase with genetic distance and are greater in telomeric than centromeric genes. Together, our results suggest that recombination is the main factor decoupling gene trees from multigenic trees. Conclusions: Our study is the first to propose a comprehensive, multigenic phylogeny of Triticeae. It clarifies several aspects of the relationships among genera and species of this tribe, and pinpoints biological groups with likely reticulate evolution. Importantly, this study extends previous results obtained in Drosophila by demonstrating that recombination can exacerbate gene-tree conflicts in phylogenetic reconstructions. Background phylogenetic trees inferred from one or a few genes can When reconstructing the phylogeny of a biological be used as proxies of the species tree. However, recent group it is implicitly assumed that species split in a studies have shown that trees inferred from different tree-like manner and that all characters (e.g., all genes genes may conflict with each other and that violation of in the genome) reveal the same genealogical history that these assumptions is more common than previously has occurred in each lineage after the split from a com- thought [1-10]. mon ancestor. When these two assumptions are met Incongruence may appear among gene trees for various reasons. If the genes used to infer the phylogenetic rela- tionships among genera and species are sampled from * Correspondence: [email protected] 1Institut National de la Recherche Agronomique, Centre de Montpellier, UMR introgressed portions of the genome produced by hybridi- Diversité et Adaptation des Plantes Cultivées, Domaine de Melgueil, 34130 zation, gene flow or horizontal gene transfer, the trees Mauguio, France obtained likely reflect the history of the introgression Full list of author information is available at the end of the article © 2011 Escobar et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Escobar et al. BMC Evolutionary Biology 2011, 11:181 Page 2 of 17 http://www.biomedcentral.com/1471-2148/11/181 rather than the history of lineage splitting [11,12]. The including the frequency of recombination, chromoso- genealogical histories of individual genes may also be mal location and evolutionary rate. misleading due to retention and stochastic sorting of ancestral polymorphisms caused by incomplete lineage Methods sorting. This is especially likely when the effective popula- Species Studied and Loci Sampled tion size of a given lineage is large with respect to the Nineteen diploid species, spanning 13 genera of Triti- time elapsed since divergence [13-15]. In this case, ceae, were analyzed. These species were selected because genetic drift is unlikely to have brought alleles to fixation they belong to most phylogenetic clades recognized so before subsequent divergence [1,6]. Finally, gene duplica- far [22,26,29] and represent most of the diversity of tion followed by gene loss may lead to incongruence diploid genera (68% according to [22] and [32]), life because paralogous gene copies are incorrectly inferred styles (annual and perennial), mating systems (self-com- to be orthologous [16]. patible and self-incompatible), and geographic origin Whatever their origin, incongruences among gene (Europe, Middle East, Asia, North America and Austra- trees require careful attention for several reasons. First, lia). One or two accessions per species were obtained they affect the interpretation of morphological and from the United States Department of Agriculture molecular patterns of evolution. Second, they maintain (USDA), National Plant Germplasm System (available at extensive instability in taxonomy. Third, they complicate http://www.ars-grin.gov/npgs/index.html), making a the choice of wild taxa as sources of novel genes in total of 32 accessions (Table 1). Although Bromus is breeding programs (e.g., genes conferring resistance to supposed to be the closest outgroup of Triticeae pathogens, tolerance to salt, low temperatures and [26,33,34], to simplify primer design we preferred to use drought). Finally, uncertainty in phylogenetic relation- Brachypodium distachyon, a more distant species for ships may lead to inadequate conservation decisions (e. which the complete genome is available [35]. As the g., the protection of particular species or habitats). ingroup topology may depend upon the choice of a sin- In prokaryotes, some authors argue that numerous gle outgroup, Zea mays and Oryza sativa were also hybridizations and gene transfers preclude the possibi- incorporated as additional, more distant outgroups. The lity and the meaning of a tree-like representation of a choice of distant outgroups may increase the number of species history [17,18]. In plants too it has been argued homoplasies. However, owing to the selective constraints that, in some cases, reticulate evolution is more appro- likely acting on the coding sequences we used (see priate than a tree-like description [19]. On the con- below), it is likely they have been affected by low substi- trary, other authors argue that despite incongruences it tutional saturation and hence by a low homoplasy level. is possible to reconstruct phylogenies and tree-like his- Orthologous coding sequences (cDNA) of one gene tories [20,21]. Among angiosperms, Triticeae grasses fragment from the chloroplast (MATK)and26nuclear provide a particularly striking example of incongruence gene fragments located on three different chromosomes among gene trees, suggesting reticulate evolution [22]. (out of the seven chromosomes representative of Triti- This tribe comprises species of major economic impor- ceae) were sequenced for each accession (Table 2; tance, including wheat, barley and rye. In recent years, GenBank: HM539308-HM540073). Sequences of B. dis- attempts to try and sort out the phylogenetic details of tachyon were obtained
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