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Multigenic phylogeny and analysis of tree incongruences in Triticeae (Poaceae).

Escobar JS, Scornavacca C, Cenci A, Guilhaumon C, Santoni S, Douzery EJ, Ranwez V, Glémin S, David J - BMC Evol. Biol. (2011)

Bottom Line: 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.Importantly, this study extends previous results obtained in Drosophila by demonstrating that recombination can exacerbate gene-tree conflicts in phylogenetic reconstructions.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut National de la Recherche Agronomique, Centre de Montpellier, UMR Diversité et Adaptation des Plantes Cultivées, Domaine de Melgueil, 34130 Mauguio, France. jsescobar2002@yahoo.fr

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.

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Supermatrix phylogeny of Triticeae. Phylogenetic tree inferred with the concatenation of 27 loci (~25 Kb). Bootstrap values are given in percentage. Maximal posterior probability (100%) for all nodes except one (indicated in brackets). Note that branch lengths of the outgroups are divided by 10 (dotted lines) in order to zoom in Triticeae.
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Figure 1: Supermatrix phylogeny of Triticeae. Phylogenetic tree inferred with the concatenation of 27 loci (~25 Kb). Bootstrap values are given in percentage. Maximal posterior probability (100%) for all nodes except one (indicated in brackets). Note that branch lengths of the outgroups are divided by 10 (dotted lines) in order to zoom in Triticeae.

Mentions: The supermatrix tree obtained with the concatenation of all loci (~25 Kb) provides a much more resolved picture than individual gene trees. ML and Bayesian analyses are consistent and produce very similar trees. According to these trees, we distinguished 5 to 7 clades depending on posterior probability or bootstrap supporting values (Figure 1). The first divergent group within Triticeae is Psathyrostachys (clade I), followed by Hordeum (clade IIA) and Pseudoroegneria (clade IIB). The internal branches are quite short compared with the terminal branches, suggesting that cladogenesis occurred in rapid succession. Two well-supported clades diverge at this point. The first is formed by Australopyrum (clade IIIA), Henrardia and Eremopyrum bonaepartis (clade IIIB), and Agropyrum and E. triticeum (clade IIIC). The second consists of Dasypyrum and Heteranthelium (clade IV), on the one hand, and Secale, Taeniatherum, Triticum and Aegilops (clade V), on the other hand.


Multigenic phylogeny and analysis of tree incongruences in Triticeae (Poaceae).

Escobar JS, Scornavacca C, Cenci A, Guilhaumon C, Santoni S, Douzery EJ, Ranwez V, Glémin S, David J - BMC Evol. Biol. (2011)

Supermatrix phylogeny of Triticeae. Phylogenetic tree inferred with the concatenation of 27 loci (~25 Kb). Bootstrap values are given in percentage. Maximal posterior probability (100%) for all nodes except one (indicated in brackets). Note that branch lengths of the outgroups are divided by 10 (dotted lines) in order to zoom in Triticeae.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3142523&req=5

Figure 1: Supermatrix phylogeny of Triticeae. Phylogenetic tree inferred with the concatenation of 27 loci (~25 Kb). Bootstrap values are given in percentage. Maximal posterior probability (100%) for all nodes except one (indicated in brackets). Note that branch lengths of the outgroups are divided by 10 (dotted lines) in order to zoom in Triticeae.
Mentions: The supermatrix tree obtained with the concatenation of all loci (~25 Kb) provides a much more resolved picture than individual gene trees. ML and Bayesian analyses are consistent and produce very similar trees. According to these trees, we distinguished 5 to 7 clades depending on posterior probability or bootstrap supporting values (Figure 1). The first divergent group within Triticeae is Psathyrostachys (clade I), followed by Hordeum (clade IIA) and Pseudoroegneria (clade IIB). The internal branches are quite short compared with the terminal branches, suggesting that cladogenesis occurred in rapid succession. Two well-supported clades diverge at this point. The first is formed by Australopyrum (clade IIIA), Henrardia and Eremopyrum bonaepartis (clade IIIB), and Agropyrum and E. triticeum (clade IIIC). The second consists of Dasypyrum and Heteranthelium (clade IV), on the one hand, and Secale, Taeniatherum, Triticum and Aegilops (clade V), on the other hand.

Bottom Line: 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.Importantly, this study extends previous results obtained in Drosophila by demonstrating that recombination can exacerbate gene-tree conflicts in phylogenetic reconstructions.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut National de la Recherche Agronomique, Centre de Montpellier, UMR Diversité et Adaptation des Plantes Cultivées, Domaine de Melgueil, 34130 Mauguio, France. jsescobar2002@yahoo.fr

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.

Show MeSH