Phylogenomic Discordance in the Eared Seals is best explained by Incomplete Lineage Sorting following Explosive Radiation in the Southern Hemisphere

AbstractThe phylogeny and systematics of fur seals and sea lions (Otariidae) have long been studied with diverse data types, including an increasing amount of molecular data. However, only a few phylogenetic relationships have reached acceptance because of strong gene-tree species tree discordance. Divergence times estimates in the group also vary largely between studies. These uncertainties impeded the understanding of the biogeographical history of the group, such as when and how trans-equatorial dispersal and subsequent speciation events occurred. Here we used high-coverage genome-wide sequencing for 14 of the 15 species of Otariidae to elucidate the phylogeny of the family and its bearing on the taxonomy and biogeographical history. Despite extreme topological discordance among gene trees, we found a fully supported species tree that agrees with the few well-accepted relationships and establishes monophyly of the genusArctocephalus. Our data support a relatively recent trans-hemispheric dispersal at the base of a southern clade, which rapidly diversified into six major lineages between 3 to 2.5 Ma.Otariadiverged first, followed byPhocarctosand then four major lineages withinArctocephalus. However, we foundZalophusto be non-monophyletic, with California(Z. californianus)and Steller sea lions(Eumetopias jubatus)grouping closer than the Galapagos sea lion (Z. wollebaeki)with evidence for introgression between the two genera. Overall, the high degree of genealogical discordance was best explained by incomplete lineage sorting resulting from quasi-simultaneous speciation within the southern clade with introgresssion playing a subordinate role in explaining the incongruence among and within prior phylogenetic studies of the family.

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Phylogenomic Discordance in the Eared Seals is best explained by Incomplete Lineage Sorting following Explosive Radiation in the Southern Hemisphere

Systematic Biology ◽

10.1093/sysbio/syaa099 ◽

2020 ◽

Author(s):

Fernando Lopes ◽

Larissa R Oliveira ◽

Amanda Kessler ◽

Yago Beux ◽

Enrique Crespo ◽

...

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Molecular Data ◽

Species Tree ◽

Gene Trees ◽

Lineage Sorting ◽

Data Types ◽

High Coverage ◽

Sea Lions ◽

The Family

Abstract The phylogeny and systematics of fur seals and sea lions (Otariidae) have long been studied with diverse data types, including an increasing amount of molecular data. However, only a few phylogenetic relationships have reached acceptance because of strong gene-tree species tree discordance. Divergence times estimates in the group also vary largely between studies. These uncertainties impeded the understanding of the biogeographical history of the group, such as when and how trans-equatorial dispersal and subsequent speciation events occurred. Here we used high-coverage genome-wide sequencing for 14 of the 15 species of Otariidae to elucidate the phylogeny of the family and its bearing on the taxonomy and biogeographical history. Despite extreme topological discordance among gene trees, we found a fully supported species tree that agrees with the few well-accepted relationships and establishes monophyly of the genus Arctocephalus. Our data support a relatively recent trans-hemispheric dispersal at the base of a southern clade, which rapidly diversified into six major lineages between 3 to 2.5 Ma. Otaria diverged first, followed by Phocarctos and then four major lineages within Arctocephalus. However, we found Zalophus to be non-monophyletic, with California (Z. californianus) and Steller sea lions (Eumetopias jubatus) grouping closer than the Galapagos sea lion (Z. wollebaeki) with evidence for introgression between the two genera. Overall, the high degree of genealogical discordance was best explained by incomplete lineage sorting resulting from quasi-simultaneous speciation within the southern clade with introgresssion playing a subordinate role in explaining the incongruence among and within prior phylogenetic studies of the family.

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How to Tackle Phylogenetic Discordance in Recent and Rapidly Radiating Groups? Developing a Workflow Using Loricaria (Asteraceae) as an Example

Frontiers in Plant Science ◽

10.3389/fpls.2021.765719 ◽

2022 ◽

Vol 12 ◽

Author(s):

Martha Kandziora ◽

Petr Sklenář ◽

Filip Kolář ◽

Roswitha Schmickl

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Species Tree ◽

Secondary Contact ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

Phylogenetic Discordance ◽

Gene Tree Discordance ◽

High Degree

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.

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Terraces in Gene Tree Reconciliation-Based Species Tree Inference

10.1101/2020.04.17.047092 ◽

2020 ◽

Author(s):

Michael J. Sanderson ◽

Michelle M. McMahon ◽

Mike Steel

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Solution Space ◽

Species Tree ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

Data Set ◽

Tree Reconciliation ◽

The Impact

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.

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Phylogenomic terraces: presence and implication in species tree estimation from gene trees

10.1101/2020.04.19.048843 ◽

2020 ◽

Author(s):

Ishrat Tanzila Farah ◽

Md Muktadirul Islam ◽

Kazi Tasnim Zinat ◽

Atif Hasan Rahman ◽

Md Shamsuzzoha Bayzid

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Species Tree ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

Deep Coalescence ◽

Tree Estimation ◽

Tree Space ◽

Multiple Species

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.

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Whole-Genome Analyses Resolve the Phylogeny of Flightless Birds (Palaeognathae) in the Presence of an Empirical Anomaly Zone

Systematic Biology ◽

10.1093/sysbio/syz019 ◽

2019 ◽

Vol 68 (6) ◽

pp. 937-955 ◽

Cited By ~ 21

Author(s):

Alison Cloutier ◽

Timothy B Sackton ◽

Phil Grayson ◽

Michele Clamp ◽

Allan J Baker ◽

...

Keyword(s):

Sequence Data ◽

Incomplete Lineage Sorting ◽

Estimation Error ◽

Gene Tree ◽

Species Tree ◽

Tree Topology ◽

Whole Genome ◽

Gene Trees ◽

Lineage Sorting ◽

Genome Analyses

Abstract Palaeognathae represent one of the two basal lineages in modern birds, and comprise the volant (flighted) tinamous and the flightless ratites. Resolving palaeognath phylogenetic relationships has historically proved difficult, and short internal branches separating major palaeognath lineages in previous molecular phylogenies suggest that extensive incomplete lineage sorting (ILS) might have accompanied a rapid ancient divergence. Here, we investigate palaeognath relationships using genome-wide data sets of three types of noncoding nuclear markers, together totaling 20,850 loci and over 41 million base pairs of aligned sequence data. We recover a fully resolved topology placing rheas as the sister to kiwi and emu + cassowary that is congruent across marker types for two species tree methods (MP-EST and ASTRAL-II). This topology is corroborated by patterns of insertions for 4274 CR1 retroelements identified from multispecies whole-genome screening, and is robustly supported by phylogenomic subsampling analyses, with MP-EST demonstrating particularly consistent performance across subsampling replicates as compared to ASTRAL. In contrast, analyses of concatenated data supermatrices recover rheas as the sister to all other nonostrich palaeognaths, an alternative that lacks retroelement support and shows inconsistent behavior under subsampling approaches. While statistically supporting the species tree topology, conflicting patterns of retroelement insertions also occur and imply high amounts of ILS across short successive internal branches, consistent with observed patterns of gene tree heterogeneity. Coalescent simulations and topology tests indicate that the majority of observed topological incongruence among gene trees is consistent with coalescent variation rather than arising from gene tree estimation error alone, and estimated branch lengths for short successive internodes in the inferred species tree fall within the theoretical range encompassing the anomaly zone. Distributions of empirical gene trees confirm that the most common gene tree topology for each marker type differs from the species tree, signifying the existence of an empirical anomaly zone in palaeognaths.

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A phylogenomic study of Steganinae fruit flies (Diptera: Drosophilidae): strong gene tree heterogeneity and evidence for monophyly

BMC Evolutionary Biology ◽

10.1186/s12862-020-01703-7 ◽

2020 ◽

Vol 20 (1) ◽

Author(s):

Guilherme Rezende Dias ◽

Eduardo Guimarães Dupim ◽

Thyago Vanderlinde ◽

Beatriz Mello ◽

Antonio Bernardo Carvalho

Keyword(s):

Gene Annotation ◽

Incomplete Lineage Sorting ◽

Branching Processes ◽

Gene Tree ◽

Morphological Characters ◽

Species Tree ◽

Small Sample ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting

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.

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wQFM: Statistically Consistent Genome-scale Species Tree Estimation from Weighted Quartets

10.1101/2020.11.30.403352 ◽

2020 ◽

Author(s):

Mahim Mahbub ◽

Zahin Wahab ◽

Rezwana Reaz ◽

M. Saifur Rahman ◽

Md. Shamsuzzoha Bayzid

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Accurate Method ◽

Species Tree ◽

Estimation Methods ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

Tree Estimation ◽

Source Form

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.

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Species Tree Estimation from Genome-wide Data with Guenomu

10.1101/023861 ◽

2015 ◽

Author(s):

Leonardo de Oliveira Martins ◽

David Posada

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Gene Families ◽

Species Tree ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

Multiple Sources ◽

Reconstruction Methods ◽

Tree Topologies

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.

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Partitioned Gene-Tree Analyses and Gene-Based Topology Testing Help Resolve Incongruence in a Phylogenomic Study of Host-Specialist Bees (Apidae: Eucerinae)

Molecular Biology and Evolution ◽

10.1093/molbev/msaa277 ◽

2020 ◽

Author(s):

Felipe V Freitas ◽

Michael G Branstetter ◽

Terry Griswold ◽

Eduardo A B Almeida

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Species Tree ◽

Data Sets ◽

Gene Trees ◽

Lineage Sorting ◽

Data Set ◽

Analytical Strategy ◽

Analytical Approaches ◽

Phylogenomic Study

Abstract Incongruence among phylogenetic results has become a common occurrence in analyses of genome-scale data sets. Incongruence originates from uncertainty in underlying evolutionary processes (e.g., incomplete lineage sorting) and from difficulties in determining the best analytical approaches for each situation. To overcome these difficulties, more studies are needed that identify incongruences and demonstrate practical ways to confidently resolve them. Here, we present results of a phylogenomic study based on the analysis 197 taxa and 2,526 ultraconserved element (UCE) loci. We investigate evolutionary relationships of Eucerinae, a diverse subfamily of apid bees (relatives of honey bees and bumble bees) with >1,200 species. We sampled representatives of all tribes within the group and >80% of genera, including two mysterious South American genera, Chilimalopsis and Teratognatha. Initial analysis of the UCE data revealed two conflicting hypotheses for relationships among tribes. To resolve the incongruence, we tested concatenation and species tree approaches and used a variety of additional strategies including locus filtering, partitioned gene-trees searches, and gene-based topological tests. We show that within-locus partitioning improves gene tree and subsequent species-tree estimation, and that this approach, confidently resolves the incongruence observed in our data set. After exploring our proposed analytical strategy on eucerine bees, we validated its efficacy to resolve hard phylogenetic problems by implementing it on a published UCE data set of Adephaga (Insecta: Coleoptera). Our results provide a robust phylogenetic hypothesis for Eucerinae and demonstrate a practical strategy for resolving incongruence in other phylogenomic data sets.

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Gene tree discord, simplex plots, and statistical tests under the coalescent

10.1101/2020.02.13.948083 ◽

2020 ◽

Cited By ~ 1

Author(s):

Elizabeth S. Allman ◽

Jonathan D. Mitchell ◽

John A. Rhodes

Keyword(s):

Incomplete Lineage Sorting ◽

Statistical Tests ◽

Gene Tree ◽

Complex Model ◽

Species Tree ◽

Data Sets ◽

Gene Trees ◽

Lineage Sorting ◽

Multispecies Coalescent ◽

Tree Inference

AbstractA simple graphical device, the simplex plot of quartet concordance factors, is introduced to aid in the exploration of a collection of gene trees on a common set of taxa. A single plot summarizes all gene tree discord, and allows for visual comparison to the expected discord from the multispecies coalescent model (MSC) of incomplete lineage sorting on a species tree. A formal statistical procedure is described that can quantify the deviation from expectation for each subset of four taxa, suggesting when the data is not in accord with the MSC, and thus either gene tree inference error is substantial or a more complex model such as that on a network may be required. If the collection of gene trees appears to be in accord with the MSC, the plots may reveal when substantial incomplete lineage sorting is present and coalescent based species tree inference is preferred over concatenation approaches. Applications to both simulated and empirical multilocus data sets illustrate the insights provided.

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