Complex patterns of reticulate evolution in opportunistic weeds (Potentilla L., Rosaceae), as revealed by low-copy nuclear markers

Background: Most cinquefoils (Potentilla L., Rosaceae) are polyploids, ranging from tetraploid (4x) to dodecaploid (12x), diploids being a rare exception. Previous studies based on ribosomal and chloroplast data indicated that Norwegian cinquefoil (P. norvegica L.) has genetic material from two separate clades within Potentilla; the Argentea and the Ivesioid clades – and thus a possible history of hybridization and polyploidization (allopolyploidy). In order to trace the putative allopolyploid origin of the species, sequence data from low-copy, biparentally inherited, nuclear markers were used. Specimens covering the circumpolar distribution of P. norvegica and its two subspecies were included, along with the morphologically similar P. intermedia. Potentilla species of low ploidy level known to belong to other relevant clades were also included. Results: Gene trees based on three low-copy nuclear markers, obtained by Bayesian Inference and Maximum Likelihood analyses, showed slightly different topologies. This is likely due to genomic reorganizations following genome duplication, but the gene trees were not in conflict with a species tree of presumably diploid taxa obtained by Multispecies Coalescent analysis. The results show that both P. norvegica and P. intermedia are allopolyploids with a shared evolutionary history involving at least four parental lineages, three from the Argentea clade and one from the Ivesioid clade. Conclusions: This is the first time that reticulate evolution has been proven in the genus Potentilla, and shows the importance of continuing working with low-copy markers in order to properly resolve its evolutionary history. Several hybridization events between the Argentea and Ivesioid clades may have given rise to the species of Wolf’s grex Rivales. To better estimate when and where these hybridizations occurred, other Argentea, Ivesioid and Rivales species should be included in future studies.publishedVersio

Detecting destabilizing species in the phylogenetic backbone of Potentilla (Rosaceae) using low-copy nuclear markers

The genus Potentilla (Rosaceae) has been subjected to several phylogenetic studies, but resolving its evolutionary history has proven challenging. Previous analyses recovered six, informally named, groups: the Argentea, Ivesioid, Fragarioides, Reptans, Alba and Anserina clades, but the relationships among some of these clades differ between data sets. The Reptans clade, which includes the type species of Potentilla, has been noticed to shift position between plastid and nuclear ribosomal data sets. We studied this incongruence by analysing four low-copy nuclear markers, in addition to chloroplast and nuclear ribosomal data, with a set of Bayesian phylogenetic and Multispecies Coalescent (MSC) analyses. A selective taxon removal strategy demonstrated that the included representatives from the Fragarioides clade, P. dickinsii and P. fragarioides, were the main sources of the instability seen in the trees. The Fragarioides species showed different relationships in each gene tree, and were only supported as a monophyletic group in a single marker when the Reptans clade was excluded from the analysis. The incongruences could not be explained by allopolyploidy, but rather by homoploid hybridization, incomplete lineage sorting or taxon sampling effects. When P. dickinsii and P. fragarioides were removed from the data set, a fully resolved, supported backbone phylogeny of Potentilla was obtained in the MSC analysis. Additionally, indications of autopolyploid origins of the Reptans and Ivesioid clades were discovered in the low-copy gene trees.publishedVersio

Complex patterns of reticulate evolution in opportunistic weeds (Potentilla L., Rosaceae), as revealed by low-copy nuclear markers

Background: Most cinquefoils (Potentilla L., Rosaceae) are polyploids, ranging from tetraploid (4x) to dodecaploid (12x), diploids being a rare exception. Previous studies based on ribosomal and chloroplast data indicated that Norwegian cinquefoil (P. norvegica L.) has genetic material from two separate clades within Potentilla; the Argentea and the Ivesioid clades – and thus a possible history of hybridization and polyploidization (allopolyploidy). In order to trace the putative allopolyploid origin of the species, sequence data from low-copy, biparentally inherited, nuclear markers were used. Specimens covering the circumpolar distribution of P. norvegica and its two subspecies were included, along with the morphologically similar P. intermedia. Potentilla species of low ploidy level known to belong to other relevant clades were also included. Results: Gene trees based on three low-copy nuclear markers, obtained by Bayesian Inference and Maximum Likelihood analyses, showed slightly different topologies. This is likely due to genomic reorganizations following genome duplication, but the gene trees were not in conflict with a species tree of presumably diploid taxa obtained by Multispecies Coalescent analysis. The results show that both P. norvegica and P. intermedia are allopolyploids with a shared evolutionary history involving at least four parental lineages, three from the Argentea clade and one from the Ivesioid clade. Conclusions: This is the first time that reticulate evolution has been proven in the genus Potentilla, and shows the importance of continuing working with low-copy markers in order to properly resolve its evolutionary history. Several hybridization events between the Argentea and Ivesioid clades may have given rise to the species of Wolf’s grex Rivales. To better estimate when and where these hybridizations occurred, other Argentea, Ivesioid and Rivales species should be included in future studies

Detecting destabilizing species in the phylogenetic backbone of Potentilla (Rosaceae) using low-copy nuclear markers

The genus Potentilla (Rosaceae) has been subjected to several phylogenetic studies, but resolving its evolutionary history has proven challenging. Previous analyses recovered six, informally named, groups: the Argentea, Ivesioid, Fragarioides, Reptans, Alba and Anserina clades, but the relationships among some of these clades differ between data sets. The Reptans clade, which includes the type species of Potentilla, has been noticed to shift position between plastid and nuclear ribosomal data sets. We studied this incongruence by analysing four low-copy nuclear markers, in addition to chloroplast and nuclear ribosomal data, with a set of Bayesian phylogenetic and Multispecies Coalescent (MSC) analyses. A selective taxon removal strategy demonstrated that the included representatives from the Fragarioides clade, P. dickinsii and P. fragarioides, were the main sources of the instability seen in the trees. The Fragarioides species showed different relationships in each gene tree, and were only supported as a monophyletic group in a single marker when the Reptans clade was excluded from the analysis. The incongruences could not be explained by allopolyploidy, but rather by homoploid hybridization, incomplete lineage sorting or taxon sampling effects. When P. dickinsii and P. fragarioides were removed from the data set, a fully resolved, supported backbone phylogeny of Potentilla was obtained in the MSC analysis. Additionally, indications of autopolyploid origins of the Reptans and Ivesioid clades were discovered in the low-copy gene trees

Correction: A Revised Time Tree of the Asterids: Establishing a Temporal Framework For Evolutionary Studies of the Coffee Family (Rubiaceae)

<p>Correction: A Revised Time Tree of the Asterids: Establishing a Temporal Framework For Evolutionary Studies of the Coffee Family (Rubiaceae)</p

A Revised Time Tree of the Asterids: Establishing a Temporal Framework For Evolutionary Studies of the Coffee Family (Rubiaceae)

<div><p>Divergence time analyses in the coffee family (Rubiaceae) have all relied on the same Gentianales crown group age estimate, reported by an earlier analysis of the asterids, for defining the upper age bound of the root node in their analyses. However, not only did the asterid analysis suffer from several analytical shortcomings, but the estimate itself has been used in highly inconsistent ways in these Rubiaceae analyses. Based on the original data, we here reanalyze the divergence times of the asterids using relaxed-clock models and 14 fossil-based minimum age constraints. We also expand the data set to include an additional 67 taxa from Rubiaceae sampled across all three subfamilies recognized in the family. Three analyses are conducted: a separate analysis of the asterids, which completely mirrors the original asterid analysis in terms of taxon sample and data; a separate analysis of the Gentianales, where the result from the first analysis is used for defining a secondary root calibration point; and a combined analysis where all taxa are analyzed simultaneously. Results are presented in the form of a time-calibrated phylogeny, and age estimates for asterid groups, Gentianales, and major groups of Rubiaceae are compared and discussed in relation to previously published estimates. Our updated age estimates for major groups of Rubiaceae provide a significant step forward towards the long term goal of establishing a robust temporal framework for the divergence of this biologically diverse and fascinating group of plants.</p></div

Fossil taxa used for specifying prior age distributions in the analyses.

<p>Note that age assignments of the fossils follow the most recent accepted ages for the sediments in which the fossils have been found, not the ages given in the original reports. Following best practice guidelines [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.ref064" target="_blank">64</a>], numerical ages assigned to different time periods correspond to their upper bounds as defined in The Geologic Time Scale 2012 [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.ref071" target="_blank">71</a>]. Node numbers refer to those indicated in (Figs <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.g001" target="_blank">1</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.g004" target="_blank">4</a>).</p><p>¹ Minimum age is constrained by radiometric dating [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.ref083" target="_blank">83</a>].</p><p>² Upper bound of the Poole Formation at the locality is 46 Myr [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.ref084" target="_blank">84</a>].</p><p>³ Bembridge Flora recently placed in the Late Eocene [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.ref085" target="_blank">85</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.ref087" target="_blank">87</a>].</p><p>Fossil taxa used for specifying prior age distributions in the analyses.</p

Chronogram of the asterids resulting from the separate analysis and calibrated against The Geologic Time Scale [71].

<p>Nodes are numbered from 1 to 180 (42 to 112; <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.g002" target="_blank">Fig 2</a>) and detailed results (mean divergence time and credibility intervals estimated by the 95% HPD) for each node is reported in the (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.s003" target="_blank">S2 Table</a>). Nodes with small black bullets are well supported in the phylogenetic analyses (BPP equal to or greater than 0.95). Ages for major groups and orders of the asterids are compared to those reported by Bremer et al. [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.ref026" target="_blank">26</a>] in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.t003" target="_blank">Table 3</a>. Credibility intervals for these nodes are indicated by red bars, and the point estimate reported by Bremer et al. [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.ref026" target="_blank">26</a>] is indicated by a light blue dot. Fossil based age estimates for selected groups are indicated by thick black bars, and these estimates were included in the analyses as uniform priors with minimum ages set to the age of the fossil (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.t002" target="_blank">Table 2</a>). Gray dots indicate the crown node position for groups that have been collapsed in the figure. The number in parenthesis next to the taxon name indicate how many taxa each of these collapsed groups included in the analysis. See (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.s002" target="_blank">S1 Table</a>) for details of all the taxa that were included in the analysis.</p

Chronogram of the Gentianales resulting from the separate analysis and calibrated against The Geologic Time Scale [71].

<p>Nodes are numbered from 42 to 112 and detailed results (mean divergence time and credibility intervals estimated by the 95% HPD) for each node is reported in the (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.s003" target="_blank">S2 Table</a>). Credibility intervals are also indicated in the figure by red bars. Nodes with small black bullets are well supported in the phylogenetic analyses (BPP equal to or greater than 0.95). Fossil based age estimates that were used in the analyses as minimum age constraints are indicated by thick black bars (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.t002" target="_blank">Table 2</a> for details). In addition a normally distributed secondary root calibration point with mean 75 Myr and standard deviation 7,7 Myr was enforced in the analysis. This secondary calibration point was based on the results from the first asterid analysis and correspond to a 95% credibility interval between 60 and 90 Myr. The three subfamilies Rubioideae, Cinchonoideae and Ixoroideae, and the Psychotrieae, Spermacoceae, Vanguerieae, and Coffeeae alliances are indicated in the tree. Current tribal assignment of each included taxa is indicated to the right of the taxon names.</p

Chronogram of the asterids resulting from the combined analysis and calibrated against The Geologic Time Scale [71].

<p>Nodes are numbered from 1 to 180 (42 to 112; <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.g004" target="_blank">Fig 4</a>) and detailed results (mean divergence time and credibility intervals estimated by the 95% HPD) for each node is reported in the (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.s003" target="_blank">S2 Table</a>). Nodes with small black bullets are well supported in the phylogenetic analyses (BPP equal to or greater than 0.95). Ages for major groups and orders of the asterids are compared to those reported by Bremer et al. [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.ref026" target="_blank">26</a>] in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.t003" target="_blank">Table 3</a>. Credibility intervals for these nodes resulting from the combined analysis are indicated by blue bars, and the point estimate reported by Bremer et al. [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.ref026" target="_blank">26</a>] is indicated by a light blue dot. Credibility intervals resulting from the separate analysis of the asterids (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.g001" target="_blank">Fig 1</a>) are included also in this figure and indicated by red bars. This provide a visualization of the differences in age estimates resulting from the two analyses. Fossil based age estimates for selected groups are indicated by thick black bars, and these estimates were included in the analyses as uniform priors with minimum ages set to the age of the fossil (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.t002" target="_blank">Table 2</a>). Gray dots indicate the crown node position for groups that have been collapsed in the figure. The number in parenthesis next to the taxon name indicate how many taxa each of these collapsed groups included in the analysis. See (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0126690#pone.0126690.s002" target="_blank">S1 Table</a>) for details of all the taxa that were included in the analysis.</p