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

Abstract

BackgroundIntrogressive 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.ResultsWe 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.ConclusionsOur 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.

Sequence variation at the three chloroplast loci (matK, rbcL, trnH-psbA) in the Triticeae tribe (Poaceae): comments on the relationships and utility in DNA barcoding of selected species

“…Moreover, the minimum-evolution dendrogram obtained on the basis of the matK sequences (Fig. 2a) revealed a close relationship between the Pseudoroegneria and the Taeniatherum clades, as well as a clear distinction of the Psathyrostachys and the Hordeum clades, which is consistent with the previous molecular studies (Fan et al 2013;Escobar et al 2011;Petersen and Seberg 1997). Thus, out of the three analyzed loci, the matK reflects intergeneric phylogenetic relationships of the Triticeae in the most complete manner.…”

“…The major clades previously defined within the Triticeae on the basis of DNA sequences are the following: (1) Psathyrostachys, (2) Hordeum, (3) Pseudoroegneria, (4) Aegilops-Triticum-Secale-Taeniatherum and (5) Eremopyrum-Agropyron-Australopyrum (Adderley and Sun 2014; Escobar et al 2011;Petersen and Seberg 1997). All of the here analyzed loci have revealed the Hordeum and Pseudoroegneria clades.…”

Dated tribe-wide whole chloroplast genome phylogeny indicates recurrent hybridizations within Triticeae

“…A sister relationship of Pseudoroegneria and Dasypyrum has been proposed recently by Escobar et al [10] based on nuclear data. In our dataset Dasypyrum groups however within Pseudoroegneria .…”

Reticulate Evolution of the Rye Genome

“…Reticulate evolution or hybrid speciation was postulated to have occurred frequently during plant evolution (Kellogg and Bennetzen, 2004;Linder and Rieseberg, 2004;Mallet, 2005). In the Triticeae, it may have occurred in diploid species (Kellogg et al, 1996;Escobar et al, 2011), but it has been most frequently postulated for allopolyploid Triticeae genera (Kellogg et al, 1996;Mason-Gamer, 2004;Mason-Gamer et al, 2010;Mahelka et al, 2011). Reticulate or hybrid speciation can occur (reviewed in Linder and Rieseberg, 2004) as a consequence of allopolyploidization, which involves fusion of unreduced gametes, or instant genome duplication after fusion of haploid gametes, giving rise to a fertile hybrid species in which diploid parental genomes are maintained.…”

“…It is important to note that reticulate genome evolution was postulated recently for rye by a multigenic phylogeny analysis (one chloroplast gene, 26 nuclear genes) of different Triticeae species (Escobar et al, 2011). Reticulate evolution or hybrid speciation was postulated to have occurred frequently during plant evolution (Kellogg and Bennetzen, 2004;Linder and Rieseberg, 2004;Mallet, 2005).…”