scholarly journals Resolving Rapid Radiations Within Angiosperm Families Using Anchored Phylogenomics

2017 ◽  
Author(s):  
Étienne Léveillé-Bourret ◽  
Julian R. Starr ◽  
Bruce A. Ford ◽  
Emily Moriarty Lemmon ◽  
Alan R. Lemmon
Keyword(s):  
Estimation Error ◽  
Gene Tree ◽  
Nuclear Gene ◽  
Nuclear Data ◽  
Pcr Primers ◽  
Nuclear Genes ◽  
Flowering Plant ◽  
Nuclear Ribosomal Dna ◽  
Anchored Phylogenomics ◽  
Rapid Radiations

AbstractDespite the promise that molecular data would provide a seemingly unlimited source of independent characters, many plant phylogenetic studies are based on only two regions, the plastid genome and nuclear ribosomal DNA (nrDNA). Their popularity can be explained by high copy numbers and universal PCR primers that make their sequences easily amplified and converted into parallel datasets. Unfortunately, their utility is limited by linked loci and limited characters resulting in low confidence in the accuracy of phylogenetic estimates, especially when rapid radiations occur. In another contribution on anchored phylogenomics in angiosperms, we presented flowering plant-specific anchored enrichment probes for hundreds of conserved nuclear genes and demonstrated their use at the level of all angiosperms. In this contribution, we focus on a common problem in phylogenetic reconstructions below the family level: weak or unresolved backbone due to rapid radiations (≤ 10 million years) followed by long divergence, using the Cariceae-Dulichieae-Scirpeae clade (CDS, Cyperaceae) as a test case. By comparing our nuclear matrix of 461 genes to a typical Sanger-sequence dataset consisting of a few plastid genes (matK, ndhF) and an nrDNA marker (ETS), we demonstrate that our nuclear data is fully compatible with the Sanger dataset and resolves short backbone internodes with high support in both concatenated and coalescence-based analyses. In addition, we show that nuclear gene tree incongruence is inversely proportional to phylogenetic information content, indicating that incongruence is mostly due to gene tree estimation error. This suggests that large numbers of conserved nuclear loci could produce more accurate trees than sampling rapidly evolving regions prone to saturation and long-branch attraction. The robust phylogenetic estimates obtained here, and high congruence with previous morphological and molecular analyses, are strong evidence for a complete tribal revision of CDS. The anchored hybrid enrichment probes used in this study should be similarly effective in other flowering plant groups. [Carex, coalescent based species tree, flowering plants, low-copy nuclear genes, low-level phylogenetics, universal hybrid enrichment probes]

scholarly journals The Perfect Storm: Gene Tree Estimation Error, Incomplete Lineage Sorting, and Ancient Gene Flow Explain the Most Recalcitrant Ancient Angiosperm Clade, Malpighiales

2020 ◽  
Author(s):  
Liming Cai ◽  
Zhenxiang Xi ◽  
Emily Moriarty Lemmon ◽  
Alan R Lemmon ◽  
Austin Mast ◽  
...  
Keyword(s):  
Gene Flow ◽  
Incomplete Lineage Sorting ◽  
Estimation Error ◽  
Gene Tree ◽  
Species Tree ◽  
Flowering Plant ◽  
Estimation Methods ◽  
Lineage Sorting ◽  
Tree Estimation ◽  
Perfect Storm

Abstract The genomic revolution offers renewed hope of resolving rapid radiations in the Tree of Life. The development of the multispecies coalescent (MSC) model and improved gene tree estimation methods can better accommodate gene tree heterogeneity caused by incomplete lineage sorting (ILS) and gene tree estimation error stemming from the short internal branches. However, the relative influence of these factors in species tree inference is not well understood. Using anchored hybrid enrichment, we generated a data set including 423 single-copy loci from 64 taxa representing 39 families to infer the species tree of the flowering plant order Malpighiales. This order includes nine of the top ten most unstable nodes in angiosperms, which have been hypothesized to arise from the rapid radiation during the Cretaceous. Here, we show that coalescent-based methods do not resolve the backbone of Malpighiales and concatenation methods yield inconsistent estimations, providing evidence that gene tree heterogeneity is high in this clade. Despite high levels of ILS and gene tree estimation error, our simulations demonstrate that these two factors alone are insufficient to explain the lack of resolution in this order. To explore this further, we examined triplet frequencies among empirical gene trees and discovered some of them deviated significantly from those attributed to ILS and estimation error, suggesting gene flow as an additional and previously unappreciated phenomenon promoting gene tree variation in Malpighiales. Finally, we applied a novel method to quantify the relative contribution of these three primary sources of gene tree heterogeneity and demonstrated that ILS, gene tree estimation error, and gene flow contributed to 10.0%, 34.8%, and 21.4% of the variation, respectively. Together, our results suggest that a perfect storm of factors likely influence this lack of resolution, and further indicate that recalcitrant phylogenetic relationships like the backbone of Malpighiales may be better represented as phylogenetic networks. Thus, reducing such groups solely to existing models that adhere strictly to bifurcating trees greatly oversimplifies reality, and obscures our ability to more clearly discern the process of evolution.

scholarly journals Targeted NGS for species level phylogenomics: “made to measure” or “one size fits all”?

PeerJ ◽  
2017 ◽  
Vol 5 ◽  
pp. e3569 ◽  
Author(s):  
Malvina Kadlec ◽  
Dirk U. Bellstedt ◽  
Nicholas C. Le Maitre ◽  
Michael D. Pirie
Keyword(s):  
High Throughput Sequencing ◽  
Gene Tree ◽  
Flowering Plant ◽  
Homologous Sequence ◽  
Gene Trees ◽  
Species Complexes ◽  
Custom Made ◽  
Targeted Ngs ◽  
Promising Source ◽  
Rapid Radiations

Targeted high-throughput sequencing using hybrid-enrichment offers a promising source of data for inferring multiple, meaningfully resolved, independent gene trees suitable to address challenging phylogenetic problems in species complexes and rapid radiations. The targets in question can either be adopted directly from more or less universal tools, or custom made for particular clades at considerably greater effort. We applied custom made scripts to select sets of homologous sequence markers from transcriptome and WGS data for use in the flowering plant genus Erica (Ericaceae). We compared the resulting targets to those that would be selected both using different available tools (Hyb-Seq; MarkerMiner), and when optimising for broader clades of more distantly related taxa (Ericales; eudicots). Approaches comparing more divergent genomes (including MarkerMiner, irrespective of input data) delivered fewer and shorter potential markers than those targeted for Erica. The latter may nevertheless be effective for sequence capture across the wider family Ericaceae. We tested the targets delivered by our scripts by obtaining an empirical dataset. The resulting sequence variation was lower than that of standard nuclear ribosomal markers (that in Erica fail to deliver a well resolved gene tree), confirming the importance of maximising the lengths of individual markers. We conclude that rather than searching for “one size fits all” universal markers, we should improve and make more accessible the tools necessary for developing “made to measure” ones.

scholarly journals Targeted NGS for species level phylogenomics: “made to measure” or “one size fits all”?

2017 ◽  
Author(s):  
Malvina Kadlec ◽  
Dirk U Bellstedt ◽  
Nicholas C Le Maitre ◽  
Michael D Pirie
Keyword(s):  
High Throughput Sequencing ◽  
Gene Tree ◽  
Flowering Plant ◽  
Homologous Sequence ◽  
Gene Trees ◽  
Species Complexes ◽  
Custom Made ◽  
Targeted Ngs ◽  
Promising Source ◽  
Rapid Radiations

Targeted high-throughput sequencing using hybrid-enrichment offers a promising source of data for inferring multiple, meaningfully resolved, independent gene trees suitable to address challenging phylogenetic problems in species complexes and rapid radiations. The targets in question can either be adopted directly from more or less universal tools, or custom made for particular clades at considerably greater effort. We applied custom made scripts to select sets of homologous sequence markers from transcriptome and WGS data for use in the flowering plant genus Erica (Ericaceae). We compared the resulting targets to those that would be selected both using different available tools (Hyb-Seq; MarkerMiner), and when optimising for broader clades of more distantly related taxa (Ericales; eudicots). Approaches comparing more divergent genomes (including MarkerMiner, irrespective of input data) delivered fewer and shorter potential markers than those targeted for Erica. The latter may nevertheless be effective for sequence capture across the wider family Ericaceae. We tested the targets delivered by our scripts by obtaining an empirical dataset. The resulting sequence variation was lower than that of standard nuclear ribosomal markers (that in Erica fail to deliver a well resolved gene tree), confirming the importance of maximising the lengths of individual markers. We conclude that rather than searching for “one size fits all” universal markers, we should improve and make more accessible the tools necessary for developing “made to measure” ones.

scholarly journals The Perfect Storm: Gene Tree Estimation Error, Incomplete Lineage Sorting, and Ancient Gene Flow Explain the Most Recalcitrant Ancient Angiosperm Clade, Malpighiales

2020 ◽  
Author(s):  
Liming Cai ◽  
Zhenxiang Xi ◽  
Emily Moriarty Lemmon ◽  
Alan R. Lemmon ◽  
Austin Mast ◽  
...  
Keyword(s):  
Gene Flow ◽  
Incomplete Lineage Sorting ◽  
Estimation Error ◽  
Gene Tree ◽  
Species Tree ◽  
Flowering Plant ◽  
Estimation Methods ◽  
Lineage Sorting ◽  
Tree Estimation ◽  
Perfect Storm

ABSTRACTThe genomic revolution offers renewed hope of resolving rapid radiations in the Tree of Life. The development of the multispecies coalescent (MSC) model and improved gene tree estimation methods can better accommodate gene tree heterogeneity caused by incomplete lineage sorting (ILS) and gene tree estimation error stemming from the short internal branches. However, the relative influence of these factors in species tree inference is not well understood. Using anchored hybrid enrichment, we generated a data set including 423 single-copy loci from 64 taxa representing 39 families to infer the species tree of the flowering plant order Malpighiales. This order alone includes nine of the top ten most unstable nodes in angiosperms, and the recalcitrant relationships along the backbone of the order have been hypothesized to arise from the rapid radiation during the Cretaceous. Here, we show that coalescent-based methods do not resolve the backbone of Malpighiales and concatenation methods yield inconsistent estimations, providing evidence that gene tree heterogeneity is high in this clade. Despite high levels of ILS and gene tree estimation error, our simulations demonstrate that these two factors alone are insufficient to explain the lack of resolution in this order. To explore this further, we examined triplet frequencies among empirical gene trees and discovered some of them deviated significantly from those attributed to ILS and estimation error, suggesting gene flow as an additional and previously unappreciated phenomenon promoting gene tree variation in Malpighiales. Finally, we applied a novel method to quantify the relative contribution of these three primary sources of gene tree heterogeneity and demonstrated that ILS, gene tree estimation error, and gene flow contributed to 15%, 52%, and 32% of the variation, respectively. Together, our results suggest that a perfect storm of factors likely influence this lack of resolution, and further indicate that recalcitrant phylogenetic relationships like the backbone of Malpighiales may be better represented as phylogenetic networks. Thus, reducing such groups solely to existing models that adhere strictly to bifurcating trees greatly oversimplifies reality, and obscures our ability to more clearly discern the process of evolution.

scholarly journals Targeted NGS for species level phylogenomics: “made to measure” or “one size fits all”?

2017 ◽  
Author(s):  
Malvina Kadlec ◽  
Dirk U Bellstedt ◽  
Nicholas C Le Maitre ◽  
Michael D Pirie
Keyword(s):  
High Throughput Sequencing ◽  
Gene Tree ◽  
Flowering Plant ◽  
Homologous Sequence ◽  
Gene Trees ◽  
Species Complexes ◽  
Custom Made ◽  
Targeted Ngs ◽  
Promising Source ◽  
Rapid Radiations

Targeted high-throughput sequencing using hybrid-enrichment offers a promising source of data for inferring multiple, meaningfully resolved, independent gene trees suitable to address challenging phylogenetic problems in species complexes and rapid radiations. The targets in question can either be adopted directly from more or less universal tools, or custom made for particular clades at considerably greater effort. We applied custom made scripts to select sets of homologous sequence markers from transcriptome and WGS data for use in the flowering plant genus Erica (Ericaceae). We compared the resulting targets to those that would be selected both using different available tools (Hyb-Seq; MarkerMiner), and when optimising for broader clades of more distantly related taxa (Ericales; eudicots). Approaches comparing more divergent genomes (including MarkerMiner, irrespective of input data) delivered fewer and shorter potential markers than those targeted for Erica. The latter may nevertheless be effective for sequence capture across the wider family Ericaceae. We tested the targets delivered by our scripts by obtaining an empirical dataset. The resulting sequence variation was lower than that of standard nuclear ribosomal markers (that in Erica fail to deliver a well resolved gene tree), confirming the importance of maximising the lengths of individual markers. We conclude that rather than searching for “one size fits all” universal markers, we should improve and make more accessible the tools necessary for developing “made to measure” ones.

scholarly journals Targeted NGS for species level phylogenomics: “made to measure” or “one size fits all”?

2017 ◽  
Author(s):  
Malvina Kadlec ◽  
Dirk U Bellstedt ◽  
Nicholas C Le Maitre ◽  
Michael D Pirie
Keyword(s):  
High Throughput Sequencing ◽  
Gene Tree ◽  
Flowering Plant ◽  
Homologous Sequence ◽  
Gene Trees ◽  
Species Complexes ◽  
Custom Made ◽  
Targeted Ngs ◽  
Promising Source ◽  
Rapid Radiations

Targeted high-throughput sequencing using hybrid-enrichment offers a promising source of data for inferring multiple, meaningfully resolved, independent gene trees suitable to address challenging phylogenetic problems in species complexes and rapid radiations. The targets in question can either be adopted directly from more or less universal tools, or custom made for particular clades at considerably greater effort. We applied custom made scripts to select sets of homologous sequence markers from transcriptome and WGS data for use in the flowering plant genus Erica (Ericaceae). We compared the resulting targets to those that would be selected both using different available tools (Hyb-Seq; MarkerMiner), and when optimising for broader clades of more distantly related taxa (Ericales; eudicots). Approaches comparing more divergent genomes (including MarkerMiner, irrespective of input data) delivered fewer and shorter potential markers than those targeted for Erica. The latter may nevertheless be effective for sequence capture across the wider family Ericaceae. We tested the targets delivered by our scripts by obtaining an empirical dataset. The resulting sequence variation was lower than that of standard nuclear ribosomal markers (that in Erica fail to deliver a well resolved gene tree), confirming the importance of maximising the lengths of individual markers. We conclude that rather than searching for “one size fits all” universal markers, we should improve and make more accessible the tools necessary for developing “made to measure” ones.

scholarly journals Targeted NGS for species level phylogenomics: “made to measure” or “one size fits all”?

2017 ◽  
Author(s):  
Malvina Kadlec ◽  
Dirk U Bellstedt ◽  
Nicholas C Le Maitre ◽  
Michael D Pirie
Keyword(s):  
High Throughput Sequencing ◽  
Gene Tree ◽  
Flowering Plant ◽  
Homologous Sequence ◽  
Gene Trees ◽  
Species Complexes ◽  
Custom Made ◽  
Targeted Ngs ◽  
Promising Source ◽  
Rapid Radiations

Targeted high-throughput sequencing using hybrid-enrichment offers a promising source of data for inferring multiple, meaningfully resolved, independent gene trees suitable to address challenging phylogenetic problems in species complexes and rapid radiations. The targets in question can either be adopted directly from more or less universal tools, or custom made for particular clades at considerably greater effort. We applied custom made scripts to select sets of homologous sequence markers from transcriptome and WGS data for use in the flowering plant genus Erica (Ericaceae). We compared the resulting targets to those that would be selected both using different available tools (Hyb-Seq; MarkerMiner), and when optimising for broader clades of more distantly related taxa (Ericales; eudicots). Approaches comparing more divergent genomes (including MarkerMiner, irrespective of input data) delivered fewer and shorter potential markers than those targeted for Erica. The latter may nevertheless be effective for sequence capture across the wider family Ericaceae. We tested the targets delivered by our scripts by obtaining an empirical dataset. The resulting sequence variation was lower than that of standard nuclear ribosomal markers (that in Erica fail to deliver a well resolved gene tree), confirming the importance of maximising the lengths of individual markers. We conclude that rather than searching for “one size fits all” universal markers, we should improve and make more accessible the tools necessary for developing “made to measure” ones.

scholarly journals Detection of cross-contamination and strong mitonuclear discordance in two species groups of sawfly genus Empria (Hymenoptera, Tenthredinidae)

2019 ◽  
Author(s):  
Marko Prous ◽  
Kyung Min Lee ◽  
Marko Mutanen
Keyword(s):  
Sanger Sequencing ◽  
Nuclear Gene ◽  
Nuclear Data ◽  
Nuclear Genes ◽  
High Rate ◽  
Coi Gene ◽  
Contamination Rate ◽  
Cross Contamination ◽  
Mitochondrial Coi ◽  
Species Groups

AbstractIn several sawfly taxa strong mitonuclear discordance has been observed, with nuclear genes supporting species assignments based on morphology, whereas the barcode region of the mitochondrial COI gene suggesting different relationships. As previous studies were based on only few nuclear genes, the causes and the degree of mitonuclear discordance remain ambiguous. Here, we obtain genomic-scale ddRAD data together with Sanger sequencing of mitochondrial COI and two to three nuclear protein coding genes to investigate species limits and mitonuclear discordance in two closely related species groups within the sawfly genus Empria. As found previously based on nuclear ITS and mitochondrial COI sequences, species are in most cases supported as monophyletic based on previous and new nuclear data reported here, but not based on mitochondrial COI. This mitonuclear discordance can be explained by occasional mitochondrial introgression with little or no nuclear gene flow, a pattern that might be common in haplodiploid taxa with slowly evolving mitochondrial genomes. Some species in E. immersa group are not recovered as monophyletic also based on nuclear data, but this could partly be because of unresolved taxonomy. Preliminary analyses of ddRAD data did not recover monophyly of E. japonica within E. longicornis group (three Sanger sequenced nuclear genes strongly supported monophyly), but closer examination of the data and additional Sanger sequencing suggested that both specimens were substantially (possibly 10–20% of recovered loci) cross-contaminated. A reason could be due to specimen identification tag jumps during sequencing library preparation of pooled specimens that in previous studies have been shown to affect up to 2.5% of the sequenced reads. We provide an R script to examine patterns of identical loci among the specimens and estimate that cross-contamination rate is not unusually high for our ddRAD dataset as a whole (based on counting identical sequences between immersa and longicornis groups that are well separated from each other and probably do not hybridise). The high rate of cross-contamination for both E. japonica specimens might be explained by small number of recovered loci (~1000) compared to most other specimens (>10 000 in some cases) because of poor sequencing results. We caution drawing unexpected biological conclusions when closely related specimens are pooled before sequencing and tagged only at one end of the molecule or at both ends using unique combination of limited number of tags (less than the number of specimens).

ITS sequence variation supports the hybrid origin of Malus toringoides Hughes

2007 ◽  
Vol 85 (7) ◽  
pp. 659-666 ◽  
Author(s):  
Ting-Ting Feng ◽  
Zhi-Qin Zhou ◽  
Jian-Min Tang ◽  
Ming-Hao Cheng ◽  
Shi-Liang Zhou
Keyword(s):  
Sequence Variation ◽  
Gene Tree ◽  
Natural Populations ◽  
Its Sequences ◽  
Nuclear Ribosomal Dna ◽  
Hybrid Origin ◽  
Putative Hybrid ◽  
Molecular Evidence ◽  
Sequence Information ◽  
Aflp Data

Malus toringoides (Rehd.) Hughes was suggested to have originated from hybridization between Malus transitoria Schneid. and Malus kansuensis Rehd., followed by repeated backcrossing to one of the putative parents. In the present study, the sequence information of the internal transcribed spacer (ITS) of nuclear ribosomal DNA (nrDNA) was used to re-examine the origin of this species. A total of 69 accessions from three natural populations (Maerkang, Xiaba and Kehe, Aba Autonomous Region, Sichuan, China) of M. toringoides and 10 accessions of its putative parents were analyzed. Using Malus angustifolia (Ait.) Michx., Malus ioensis (Wood) Britt. and Malus doumeri Chev. as outgroups, our phylogenetic analysis of the ITS sequences of M. toringoides and its putative parents showed that M. toringoides was not monophyletic, and two different types of ITS sequences which were obtained from each of the six accessions of M. toringoides were found to have clustered separately with those of the two putative parent species on the gene tree. A comparison of the sequence variation between M. toringoides and its putative parents revealed an additive variation pattern of ITS sequences in the putative hybrid species. These results are consistent with the previous morphological and amplified fragment length polymorphism (AFLP) data which suggested that M. toringoides was of hybrid origin. Our ITS data provide new molecular evidence for the hybrid origin hypothesis of M. toringoides and these results are of great importance for future study on hybridization, polyploid speciation and evolution of the genus Malus Miller.

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