scholarly journals Phylogenomic data reveal hard polytomies across the backbone of the large genus Solanum (Solanaceae)

2021 ◽  
Author(s):  
Edeline Gagnon ◽  
Rebecca Hilgenhof ◽  
Andr&eacutes Orejuela ◽  
Angela McDonnell ◽  
Gaurav Sablok ◽  
...  

Increased volumes of phylogenomic data have revealed incongruent topologies in gene trees, both between and within genomes across many organisms. Some of these incongruences indicate polytomies that may remain impossible to resolve. Here, widespread gene-tree discordance is uncovered along the backbone of Solanum, one of the largest flowering plant genera that includes the cultivated potato, tomato, and eggplant, as well as 24 minor crop plants. First, a densely sampled species-level phylogeny of Solanum is built using unpublished and publicly available Sanger sequences comprising 60% of all accepted species (742 spp.) and nine regions (ITS, waxy, and seven plastid markers). The robustness of the Sanger-based topology is tested by examining a plastome dataset with 140 species and a nuclear target-capture dataset with 39 species of Solanum. Clear incongruences between species trees generated from the supermatrix, plastome, and nuclear target-capture datasets are revealed. Discordance within the plastome and target-capture dataset are found at different evolutionary depths in three different areas along the backbone of these phylogenetic trees, with polytomy tests suggesting that most of these nodes have short branches and should be collapsed. We argue that incomplete lineage sorting due to rapid diversification is the most likely cause behind these polytomies, and that embracing the uncertainty that underlies them is crucial to depict the evolution of large and rapidly radiating lineages.

2022 ◽  
Vol 12 ◽  
Author(s):  
Martha Kandziora ◽  
Petr Sklenář ◽  
Filip Kolář ◽  
Roswitha Schmickl

A major challenge in phylogenetics and -genomics is to resolve young rapidly radiating groups. The fast succession of species increases the probability of incomplete lineage sorting (ILS), and different topologies of the gene trees are expected, leading to gene tree discordance, i.e., not all gene trees represent the species tree. Phylogenetic discordance is common in phylogenomic datasets, and apart from ILS, additional sources include hybridization, whole-genome duplication, and methodological artifacts. Despite a high degree of gene tree discordance, species trees are often well supported and the sources of discordance are not further addressed in phylogenomic studies, which can eventually lead to incorrect phylogenetic hypotheses, especially in rapidly radiating groups. We chose the high-Andean Asteraceae genus Loricaria to shed light on the potential sources of phylogenetic discordance and generated a phylogenetic hypothesis. By accounting for paralogy during gene tree inference, we generated a species tree based on hundreds of nuclear loci, using Hyb-Seq, and a plastome phylogeny obtained from off-target reads during target enrichment. We observed a high degree of gene tree discordance, which we found implausible at first sight, because the genus did not show evidence of hybridization in previous studies. We used various phylogenomic analyses (trees and networks) as well as the D-statistics to test for ILS and hybridization, which we developed into a workflow on how to tackle phylogenetic discordance in recent radiations. We found strong evidence for ILS and hybridization within the genus Loricaria. Low genetic differentiation was evident between species located in different Andean cordilleras, which could be indicative of substantial introgression between populations, promoted during Pleistocene glaciations, when alpine habitats shifted creating opportunities for secondary contact and hybridization.


Author(s):  
Diego F Morales-Briones ◽  
Gudrun Kadereit ◽  
Delphine T Tefarikis ◽  
Michael J Moore ◽  
Stephen A Smith ◽  
...  

Abstract Gene tree discordance in large genomic data sets can be caused by evolutionary processes such as incomplete lineage sorting and hybridization, as well as model violation, and errors in data processing, orthology inference, and gene tree estimation. Species tree methods that identify and accommodate all sources of conflict are not available, but a combination of multiple approaches can help tease apart alternative sources of conflict. Here, using a phylotranscriptomic analysis in combination with reference genomes, we test a hypothesis of ancient hybridization events within the plant family Amaranthaceae s.l. that was previously supported by morphological, ecological, and Sanger-based molecular data. The data set included seven genomes and 88 transcriptomes, 17 generated for this study. We examined gene-tree discordance using coalescent-based species trees and network inference, gene tree discordance analyses, site pattern tests of introgression, topology tests, synteny analyses, and simulations. We found that a combination of processes might have generated the high levels of gene tree discordance in the backbone of Amaranthaceae s.l. Furthermore, we found evidence that three consecutive short internal branches produce anomalous trees contributing to the discordance. Overall, our results suggest that Amaranthaceae s.l. might be a product of an ancient and rapid lineage diversification, and remains, and probably will remain, unresolved. This work highlights the potential problems of identifiability associated with the sources of gene tree discordance including, in particular, phylogenetic network methods. Our results also demonstrate the importance of thoroughly testing for multiple sources of conflict in phylogenomic analyses, especially in the context of ancient, rapid radiations. We provide several recommendations for exploring conflicting signals in such situations. [Amaranthaceae; gene tree discordance; hybridization; incomplete lineage sorting; phylogenomics; species network; species tree; transcriptomics.]


2020 ◽  
Author(s):  
Michael J. Sanderson ◽  
Michelle M. McMahon ◽  
Mike Steel

AbstractTerraces in phylogenetic tree space are sets of trees with identical optimality scores for a given data set, arising from missing data. These were first described for multilocus phylogenetic data sets in the context of maximum parsimony inference and maximum likelihood inference under certain model assumptions. Here we show how the mathematical properties that lead to terraces extend to gene tree - species tree problems in which the gene trees are incomplete. Inference of species trees from either sets of gene family trees subject to duplication and loss, or allele trees subject to incomplete lineage sorting, can exhibit terraces in their solution space. First, we show conditions that lead to a new kind of terrace, which stems from subtree operations that appear in reconciliation problems for incomplete trees. Then we characterize when terraces of both types can occur when the optimality criterion for tree search is based on duplication, loss or deep coalescence scores. Finally, we examine the impact of assumptions about the causes of losses: whether they are due to imperfect sampling or true evolutionary deletion.


2020 ◽  
Author(s):  
Ishrat Tanzila Farah ◽  
Md Muktadirul Islam ◽  
Kazi Tasnim Zinat ◽  
Atif Hasan Rahman ◽  
Md Shamsuzzoha Bayzid

AbstractSpecies tree estimation from multi-locus dataset is extremely challenging, especially in the presence of gene tree heterogeneity across the genome due to incomplete lineage sorting (ILS). Summary methods have been developed which estimate gene trees and then combine the gene trees to estimate a species tree by optimizing various optimization scores. In this study, we have formalized the concept of “phylogenomic terraces” in the species tree space, where multiple species trees with distinct topologies may have exactly the same optimization score (quartet score, extra lineage score, etc.) with respect to a collection of gene trees. We investigated the presence and implication of terraces in species tree estimation from multi-locus data by taking ILS into account. We analyzed two of the most popular ILS-aware optimization criteria: maximize quartet consistency (MQC) and minimize deep coalescence (MDC). Methods based on MQC are provably statistically consistent, whereas MDC is not a consistent criterion for species tree estimation. Our experiments, on a collection of dataset simulated under ILS, indicate that MDC-based methods may achieve competitive or identical quartet consistency score as MQC but could be significantly worse than MQC in terms of tree accuracy – demonstrating the presence and affect of phylogenomic terraces. This is the first known study that formalizes the concept of phylogenomic terraces in the context of species tree estimation from multi-locus data, and reports the presence and implications of terraces in species tree estimation under ILS.


2020 ◽  
Vol 20 (1) ◽  
Author(s):  
Guilherme Rezende Dias ◽  
Eduardo Guimarães Dupim ◽  
Thyago Vanderlinde ◽  
Beatriz Mello ◽  
Antonio Bernardo Carvalho

Abstract Background The Drosophilidae family is traditionally divided into two subfamilies: Drosophilinae and Steganinae. This division is based on morphological characters, and the two subfamilies have been treated as monophyletic in most of the literature, but some molecular phylogenies have suggested Steganinae to be paraphyletic. To test the paraphyletic-Steganinae hypothesis, here, we used genomic sequences of eight Drosophilidae (three Steganinae and five Drosophilinae) and two Ephydridae (outgroup) species and inferred the phylogeny for the group based on a dataset of 1,028 orthologous genes present in all species (> 1,000,000 bp). This dataset includes three genera that broke the monophyly of the subfamilies in previous works. To investigate possible biases introduced by small sample sizes and automatic gene annotation, we used the same methods to infer species trees from a set of 10 manually annotated genes that are commonly used in phylogenetics. Results Most of the 1,028 gene trees depicted Steganinae as paraphyletic with distinct topologies, but the most common topology depicted it as monophyletic (43.7% of the gene trees). Despite the high levels of gene tree heterogeneity observed, species tree inference in ASTRAL, in PhyloNet, and with the concatenation approach strongly supported the monophyly of both subfamilies for the 1,028-gene dataset. However, when using the concatenation approach to infer a species tree from the smaller set of 10 genes, we recovered Steganinae as a paraphyletic group. The pattern of gene tree heterogeneity was asymmetrical and thus could not be explained solely by incomplete lineage sorting (ILS). Conclusions Steganinae was clearly a monophyletic group in the dataset that we analyzed. In addition to ILS, gene tree discordance was possibly the result of introgression, suggesting complex branching processes during the early evolution of Drosophilidae with short speciation intervals and gene flow. Our study highlights the importance of genomic data in elucidating contentious phylogenetic relationships and suggests that phylogenetic inference for drosophilids based on small molecular datasets should be performed cautiously. Finally, we suggest an approach for the correction and cleaning of BUSCO-derived genomic datasets that will be useful to other researchers planning to use this tool for phylogenomic studies.


2019 ◽  
Author(s):  
Diego F. Morales-Briones ◽  
Gudrun Kadereit ◽  
Delphine T. Tefarikis ◽  
Michael J. Moore ◽  
Stephen A. Smith ◽  
...  

AbstractGene tree discordance in large genomic datasets can be caused by evolutionary processes such as incomplete lineage sorting and hybridization, as well as model violation, and errors in data processing, orthology inference, and gene tree estimation. Species tree methods that identify and accommodate all sources of conflict are not available, but a combination of multiple approaches can help tease apart alternative sources of conflict. Here, using a phylotranscriptomic analysis in combination with reference genomes, we test a hypothesis of ancient hybridization events within the plant family Amaranthaceae s.l. that was previously supported by morphological, ecological, and Sanger-based molecular data. The dataset included seven genomes and 88 transcriptomes, 17 generated for this study. We examined gene-tree discordance using coalescent-based species trees and network inference, gene tree discordance analyses, site pattern tests of introgression, topology tests, synteny analyses, and simulations. We found that a combination of processes might have generated the high levels of gene tree discordance in the backbone of Amaranthaceae s.l. Furthermore, we found evidence that three consecutive short internal branches produce anomalous trees contributing to the discordance. Overall, our results suggest that Amaranthaceae s.l. might be a product of an ancient and rapid lineage diversification, and remains, and probably will remain, unresolved. This work highlights the potential problems of identifiability associated with the sources of gene tree discordance including, in particular, phylogenetic network methods. Our results also demonstrate the importance of thoroughly testing for multiple sources of conflict in phylogenomic analyses, especially in the context of ancient, rapid radiations. We provide several recommendations for exploring conflicting signals in such situations.


2020 ◽  
Author(s):  
Mahim Mahbub ◽  
Zahin Wahab ◽  
Rezwana Reaz ◽  
M. Saifur Rahman ◽  
Md. Shamsuzzoha Bayzid

AbstractMotivationSpecies tree estimation from genes sampled from throughout the whole genome is complicated due to the gene tree-species tree discordance. Incomplete lineage sorting (ILS) is one of the most frequent causes for this discordance, where alleles can coexist in populations for periods that may span several speciation events. Quartet-based summary methods for estimating species trees from a collection of gene trees are becoming popular due to their high accuracy and statistical guarantee under ILS. Generating quartets with appropriate weights, where weights correspond to the relative importance of quartets, and subsequently amalgamating the weighted quartets to infer a single coherent species tree allows for a statistically consistent way of estimating species trees. However, handling weighted quartets is challenging.ResultsWe propose wQFM, a highly accurate method for species tree estimation from multi-locus data, by extending the quartet FM (QFM) algorithm to a weighted setting. wQFM was assessed on a collection of simulated and real biological datasets, including the avian phylogenomic dataset which is one of the largest phylogenomic datasets to date. We compared wQFM with wQMC, which is the best alternate method for weighted quartet amalgamation, and with ASTRAL, which is one of the most accurate and widely used coalescent-based species tree estimation methods. Our results suggest that wQFM matches or improves upon the accuracy of wQMC and ASTRAL.AvailabilitywQFM is available in open source form at https://github.com/Mahim1997/wQFM-2020.


2015 ◽  
Author(s):  
Leonardo de Oliveira Martins ◽  
David Posada

The history of particular genes and that of the species that carry them can be different due to different reasons. In particular, gene trees and species trees can truly differ due to well-known evolutionary processes like gene duplication and loss, lateral gene transfer or incomplete lineage sorting. Different species tree reconstruction methods have been developed to take this incongruence into account, which can be divided grossly into supertree and supermatrix approaches. Here, we introduce a new Bayesian hierarchical model that we have recently developed and implemented in the program Guenomu, that considers multiple sources of gene tree/species tree disagreement. Guenomu takes as input the posterior distributions of unrooted gene tree topologies for multiple gene families, in order to estimate the posterior distribution of rooted species tree topologies.


2020 ◽  
Author(s):  
Qiuyi Li ◽  
Celine Scornavacca ◽  
Nicolas Galtier ◽  
Yao-Ban Chan

Abstract Incomplete lineage sorting (ILS), the interaction between coalescence and speciation, can generate incongruence between gene trees and species trees, as can gene duplication (D), transfer (T) and loss (L). These processes are usually modelled independently, but in reality, ILS can affect gene copy number polymorphism, i.e., interfere with DTL. This has been previously recognised, but not treated in a satisfactory way, mainly because DTL events are naturally modelled forward-in-time, while ILS is naturally modelled backwards-in-time with the coalescent. Here we consider the joint action of ILS and DTL on the gene tree/species tree problem in all its complexity. In particular, we show that the interaction between ILS and duplications/transfers (without losses) can result in patterns usually interpreted as resulting from gene loss, and that the realised rate of D, T and L becomes non-homogeneous in time when ILS is taken into account. We introduce algorithmic solutions to these problems. Our new model, the multilocus multispecies coalescent (MLMSC), which also accounts for any level of linkage between loci, generalises the multispecies coalescent model and offers a versatile, powerful framework for proper simulation and inference of gene family evolution.


2015 ◽  
Author(s):  
Diego Mallo ◽  
Leonardo de Oliveira Martins ◽  
David Posada

We present here a fast and flexible software–SimPhy–for the simulation of multiple gene families evolving under incomplete lineage sorting, gene duplication and loss, horizontal gene transfer—all three potentially leading to the species tree/gene tree discordance—and gene conversion. SimPhy implements a hierarchical phylogenetic model in which the evolution of species, locus and gene trees is governed by global and local parameters (e.g., genome-wide, species-specific, locus-specific), that can be fixed or be sampled from a priori statistical distributions. SimPhy also incorporates comprehensive models of substitution rate variation among lineages (uncorrelated relaxed clocks) and the capability of simulating partitioned nucleotide, codon and protein multilocus sequence alignments under a plethora of substitution models using the program INDELible. We validate SimPhy's output using theoretical expectations and other programs, and show that it scales extremely well with complex models and/or large trees, being an order of magnitude faster than the most similar program (DLCoal-Sim). In addition, we demonstrate how SimPhy can be useful to understand interactions among different evolutionary processes, conducting a simulation study to characterize the systematic overestimation of the duplication time when using standard reconciliation methods. SimPhy is available at https://github.com/adamallo/SimPhy, where users can find the source code, pre-compiled executables, a detailed manual and example cases.


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