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

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.

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.

Figure 2

Primary concordance tree of Triticeae. Phylogenetic tree inferred with BUCKy. Splits are presented in branches. Concordance factors for splits are presented in Table 4. Clades named as in Figure 1.

Figure 3

Multigenic network of Triticeae. Network obtained from the 27 individual gene trees modified with PhySIC_IST [56] using a correction threshold of 0.9 (see details in Methods).

Figure 4

Effect of recombination on incongruences. A. Incongruence level of loci located in centromeres (filled bars) and telomeres (open bars). B. Correlation between the triplet distance and genetic distance between pairs of loci. Only loci located on chromosome 3 are depicted.

Figure 5

Effect of recombination on incongruences. Relationship between the triplet distance between individual gene trees and the two multigenic trees (supermatrix tree in A; BUCKy tree in B) as a function of the genetic distance between genes located on chromosome 3. The triplet distance between individual gene trees and the multigenic trees is the percentage of triplets of accessions that were resolved differently by a multigenic tree and a given gene tree. Solid line: best fit using all points; dashed line: best fit without a potential outlier (filled point). The genetic distance is connected to the chromosomal position according to the schematic diagram presented in C (red point: centromere; dark blue: centromeric regions; light blue: telomeric regions). D. Degree of incongruence among pairs of loci relative to the genetic distance on chromosome 3. Colors represent the degree of incongruence (white: no incongruence; red: strongest incongruence).