Overtraining often results in topologically incorrect species trees with maximum likelihood methods

AbstractBackgroundOvertraining occurs when an optimization process is applied for too many steps, leading to a model describing noise in addition to the signal present in the data. This effect may affect typical approaches for species tree reconstruction that use maximum likelihood optimization procedures on a small sample of concatenated genes. In this context, overtraining may result in trees better describing the specific evolutionary history of the sampled genes rather than the sought evolutionary relationships among the species.ResultsUsing a cross-validation-like approach on real and simulated datasets we showed that overtraining occurs in a significant fraction of cases, leading to species trees that are more distant from a gold-standard reference tree than a previously considered (and rejected) solution in the optimization process. However, we show that the shape of the likelihood curve is informative of the optimal stopping point. As expected, overtraining is aggravated in smaller gene samples and in datasets with increased levels of topological variation among gene trees, but occurs also in controlled, simulated scenarios where a common underlying topology is enforced.ConclusionsOvertraining is frequent in species tree reconstruction and leads to a final tree that is worse in describing the evolutionary relationships of the species under study than an earlier (and rejected) solution encountered during the likelihood optimization process. This result should help develop specific methods for species tree reconstruction in the future, and may improve our understanding of the complexity of tree likelihood landscapes.

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Genomic Characterization and Curation of UCEs Improves Species Tree Reconstruction

Systematic Biology ◽

10.1093/sysbio/syaa063 ◽

2020 ◽

Author(s):

Matthew H Van Dam ◽

James B Henderson ◽

Lauren Esposito ◽

Michelle Trautwein

Keyword(s):

Marine Invertebrates ◽

Phylogenetic Analyses ◽

Single Gene ◽

Gene Tree ◽

Single Copy ◽

Species Tree ◽

Bootstrap Support ◽

Gene Trees ◽

Species Trees ◽

Tree Reconstruction

Abstract Ultraconserved genomic elements (UCEs) are generally treated as independent loci in phylogenetic analyses. The identification pipeline for UCE probes does not require prior knowledge of genetic identity, only selecting loci that are highly conserved, single copy, without repeats, and of a particular length. Here, we characterized UCEs from 11 phylogenomic studies across the animal tree of life, from birds to marine invertebrates. We found that within vertebrate lineages, UCEs are mostly intronic and intergenic, while in invertebrates, the majority are in exons. We then curated four different sets of UCE markers by genomic category from five different studies including: birds, mammals, fish, Hymenoptera (ants, wasps, and bees), and Coleoptera (beetles). Of genes captured by UCEs, we find that many are represented by two or more UCEs, corresponding to nonoverlapping segments of a single gene. We considered these UCEs to be nonindependent, merged all UCEs that belonged to a particular gene, constructed gene and species trees, and then evaluated the subsequent effect of merging cogenic UCEs on gene and species tree reconstruction. Average bootstrap support for merged UCE gene trees was significantly improved across all data sets apparently driven by the increase in loci length. Additionally, we conducted simulations and found that gene trees generated from merged UCEs were more accurate than those generated by unmerged UCEs. As loci length improves gene tree accuracy, this modest degree of UCE characterization and curation impacts downstream analyses and demonstrates the advantages of incorporating basic genomic characterizations into phylogenomic analyses. [Anchored hybrid enrichment; ants; ASTRAL; bait capture; carangimorph; Coleoptera; conserved nonexonic elements; exon capture; gene tree; Hymenoptera; mammal; phylogenomic markers; songbird; species tree; ultraconserved elements; weevils.]

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Genomic characterization and curation of UCEs improves species tree reconstruction

10.1101/828335 ◽

2019 ◽

Author(s):

Matthew H. Van Dam ◽

James B. Henderson ◽

Lauren Esposito ◽

Michelle Trautwein

Keyword(s):

Marine Invertebrates ◽

Phylogenetic Analyses ◽

Single Gene ◽

Single Copy ◽

Species Tree ◽

Bootstrap Support ◽

Gene Trees ◽

Species Trees ◽

Tree Reconstruction ◽

Phylogenomic Analyses

ABSTRACTUltraconserved genomic elements (UCEs), are generally treated as independent loci in phylogenetic analyses. The identification pipeline for UCE probes is agnostic to genetic identity, only selecting loci that are highly conserved, single copy, without repeats, and of a particular length. Here we characterized UCEs from 12 phylogenomic studies across the animal tree of life, from birds to marine invertebrates. We found that within vertebrate lineages, UCEs are mostly intronic and intergenic, while in invertebrates, the majority are in exons. We then curated 4 different sets of UCE markers by genomic category from 5 different studies including; birds, mammals, fish, Hymenoptera (ants, wasps and bees) and Coleoptera (beetles). Of genes captured by UCEs, we find that many are represented by 2 or more UCEs, corresponding to non-overlapping segments of a single gene. We considered these UCEs to be non-independent, merged all UCEs that belonged to a particular gene, constructed gene and species trees, and then evaluated the subsequent effect of merging co-genic UCEs on gene and species tree reconstruction. Average bootstrap support for merged UCE gene trees were significantly improved across all datasets. Increased loci length appears to drive this increase in bootstrap support. Additionally, we found that gene trees generated from merged UCEs were more accurate than those generated by unmerged and randomly merged UCEs, based on our simulation study. This modest degree of UCE characterization and curation impacts downstream analyses and demonstrates the advantages of incorporating basic genomic characterizations into phylogenomic analyses.

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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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INSTRAL: Discordance-Aware Phylogenetic Placement Using Quartet Scores

Systematic Biology ◽

10.1093/sysbio/syz045 ◽

2019 ◽

Vol 69 (2) ◽

pp. 384-391 ◽

Cited By ~ 1

Author(s):

Maryam Rabiee ◽

Siavash Mirarab

Keyword(s):

New Species ◽

De Novo ◽

Gene Tree ◽

Species Tree ◽

Gene Trees ◽

Species Trees ◽

Tree Reconstruction ◽

Phylogenetic Placement ◽

Human Effort ◽

Phylogenomic Analyses

Abstract Phylogenomic analyses have increasingly adopted species tree reconstruction using methods that account for gene tree discordance using pipelines that require both human effort and computational resources. As the number of available genomes continues to increase, a new problem is facing researchers. Once more species become available, they have to repeat the whole process from the beginning because updating species trees is currently not possible. However, the de novo inference can be prohibitively costly in human effort or machine time. In this article, we introduce INSTRAL, a method that extends ASTRAL to enable phylogenetic placement. INSTRAL is designed to place a new species on an existing species tree after sequences from the new species have already been added to gene trees; thus, INSTRAL is complementary to existing placement methods that update gene trees. [ASTRAL; ILS; phylogenetic placement; species tree reconstruction.]

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Maximum Likelihood Estimation of Species Trees from Gene Trees in the Presence of Ancestral Population Structure

Genome Biology and Evolution ◽

10.1093/gbe/evaa022 ◽

2020 ◽

Vol 12 (2) ◽

pp. 3977-3995 ◽

Cited By ~ 1

Author(s):

Hillary Koch ◽

Michael DeGiorgio

Keyword(s):

Population Structure ◽

Maximum Likelihood ◽

Gene Tree ◽

Species Tree ◽

Ease Of Use ◽

Likelihood Method ◽

Ancestral Population ◽

Gene Trees ◽

Species Trees ◽

Data Set

Abstract Though large multilocus genomic data sets have led to overall improvements in phylogenetic inference, they have posed the new challenge of addressing conflicting signals across the genome. In particular, ancestral population structure, which has been uncovered in a number of diverse species, can skew gene tree frequencies, thereby hindering the performance of species tree estimators. Here we develop a novel maximum likelihood method, termed TASTI (Taxa with Ancestral structure Species Tree Inference), that can infer phylogenies under such scenarios, and find that it has increasing accuracy with increasing numbers of input gene trees, contrasting with the relatively poor performances of methods not tailored for ancestral structure. Moreover, we propose a supertree approach that allows TASTI to scale computationally with increasing numbers of input taxa. We use genetic simulations to assess TASTI’s performance in the three- and four-taxon settings and demonstrate the application of TASTI on a six-species Afrotropical mosquito data set. Finally, we have implemented TASTI in an open-source software package for ease of use by the scientific community.

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Statistical inconsistency of the unrooted minimize deep coalescence criterion

PLoS ONE ◽

10.1371/journal.pone.0251107 ◽

2021 ◽

Vol 16 (5) ◽

pp. e0251107

Author(s):

Ayed A. R. Alanzi ◽

James H. Degnan

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Species Tree ◽

Evolutionary Relationships ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

Input Gene ◽

Multispecies Coalescent ◽

Deep Coalescence

Species trees, which describe the evolutionary relationships between species, are often inferred from gene trees, which describe the ancestral relationships between sequences sampled at different loci from the species of interest. A common approach to inferring species trees from gene trees is motivated by supposing that gene tree variation is due to incomplete lineage sorting, also known as deep coalescence. One of the earliest methods motivated by deep coalescence is to find the species tree that minimizes the number of deep coalescent events needed to explain discrepancies between the species tree and input gene trees. This minimize deep coalescence (MDC) criterion can be applied in both rooted and unrooted settings. where either rooted or unrooted gene trees can be used to infer a rooted species tree. Previous work has shown that MDC is statistically inconsistent in the rooted setting, meaning that under a probabilistic model for deep coalescence, the multispecies coalescent, for some species trees, increasing the number of input gene trees does not make the method more likely to return a correct species tree. Here, we obtain analogous results in the unrooted setting, showing conditions leading to inconsistency of the MDC criterion using the multispecies coalescent model with unrooted gene trees for four taxa and five taxa.

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Impact of Ghost Introgression on Coalescent-based Species Tree Inference and Estimation of Divergence Time

10.1101/2022.01.11.475787 ◽

2022 ◽

Author(s):

XiaoXu Pang ◽

Da-Yong Zhang

Keyword(s):

Incomplete Lineage Sorting ◽

Divergence Time ◽

Species Tree ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

Multispecies Coalescent ◽

Tree Inference ◽

Tree Methods ◽

The Impact

The species studied in any evolutionary investigation generally constitute a very small proportion of all the species currently existing or that have gone extinct. It is therefore likely that introgression, which is widespread across the tree of life, involves "ghosts," i.e., unsampled, unknown, or extinct lineages. However, the impact of ghost introgression on estimations of species trees has been rarely studied and is thus poorly understood. In this study, we use mathematical analysis and simulations to examine the robustness of species tree methods based on a multispecies coalescent model under gene flow sourcing from an extant or ghost lineage. We found that very low levels of extant or ghost introgression can result in anomalous gene trees (AGTs) on three-taxon rooted trees if accompanied by strong incomplete lineage sorting (ILS). In contrast, even massive introgression, with more than half of the recipient genome descending from the donor lineage, may not necessarily lead to AGTs. In cases involving an ingroup lineage (defined as one that diverged no earlier than the most basal species under investigation) acting as the donor of introgression, the time of root divergence among the investigated species was either underestimated or remained unaffected, but for the cases of outgroup ghost lineages acting as donors, the divergence time was generally overestimated. Under many conditions of ingroup introgression, the stronger the ILS was, the higher was the accuracy of estimating the time of root divergence, although the topology of the species tree is more prone to be biased by the effect of introgression.

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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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SpeciesRax: A tool for maximum likelihood species tree inference from gene family trees under duplication, transfer, and loss.

10.1101/2021.03.29.437460 ◽

2021 ◽

Author(s):

Benoit Morel ◽

Paul Schade ◽

Sarah Lutteropp ◽

Tom A. Williams ◽

Gergely J. Szöllösi ◽

...

Keyword(s):

Maximum Likelihood ◽

Gene Family ◽

Gene Families ◽

Species Tree ◽

Likelihood Method ◽

Gene Trees ◽

Informative Signal ◽

Tree Inference ◽

Species Tree Inference ◽

Family Trees

Species tree inference from gene family trees is becoming increasingly popular because it can account for discordance between the species tree and the corresponding gene family trees. In particular, methods that can account for multiple-copy gene families exhibit potential to leverage paralogy as informative signal. At present, there does not exist any widely adopted inference method for this purpose. Here, we present SpeciesRax, the first maximum likelihood method that can infer a rooted species tree from a set of gene family trees and can account for gene duplication, loss, and transfer events. By explicitly modelling events by which gene trees can depart from the species tree, SpeciesRax leverages the phylogenetic rooting signal in gene trees. SpeciesRax infers species tree branch lengths in units of expected substitutions per site and branch support values via paralogy-aware quartets extracted from the gene family trees. Using both empirical and simulated datasets we show that SpeciesRax is at least as accurate as the best competing methods while being one order of magnitude faster on large datasets at the same time. We used SpeciesRax to infer a biologically plausible rooted phylogeny of the vertebrates comprising $188$ species from $31612$ gene families in one hour using $40$ cores. SpeciesRax is available under GNU GPL at https://github.com/BenoitMorel/GeneRax and on BioConda.

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From population genetics to phylogeny: Uses and limits of mitochondrial DNA

Australian Systematic Botany ◽

10.1071/sb9900111 ◽

1990 ◽

Vol 3 (1) ◽

pp. 111 ◽

Cited By ~ 9

Author(s):

RH Crozier

Keyword(s):

Mitochondrial Dna ◽

Mitochondrial Gene ◽

Single Gene ◽

Dna Amplification ◽

Species Tree ◽

Population Subdivision ◽

Evolutionary Divergence ◽

Gene Trees ◽

Species Trees ◽

Effective Population

Mitochondrial DNA (mtDNA) is clonally and maternally inherited in all animals and in most plants. Mitochondrial gene content is similar although not identical in all eukaryotes. Because of these characteristics, mtDNA has a number of features useful to systematists for all levels of evolutionary divergence. Clonal inheritance leads to unusual confidence in constructing gene trees which are useful in population-level studies, such as in the detection of population subdivision. Maternal inheritance presents the opportunity to distinguish paternal from maternal gene flow. The clonal, or single-gene, nature of mtDNA inheritance leads to consideration of the expected convergence between gene- and species-trees. For closely related populations or species, it is desirable to use several genes to be sure that the correct species-tree is discovered; this means that, although mtDNA will be the most precise guide to the species tree because of its lower effective population size, nuclear genes should also be used in such studies. Although restriction fragment length polymorphisms dominated the field until recently, sequencing following DNA amplification using the polymerase chain reaction is now easier and opens up the use of preserved specimens to molecular systematists. Because mitochondria1 genes evolve at different rates, one of appropriate rate can be selected for almost any phylogenetic problem.

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