Multiple nuclear genes and retroposons support vicariance and dispersal of the palaeognaths, and an Early Cretaceous origin of modern birds

The origin and timing of the diversification of modern birds remains controversial, primarily because phylogenetic relationships are incompletely resolved and uncertainty persists in molecular estimates of lineage ages. Here, we present a species tree for the major palaeognath lineages using 27 nuclear genes and 27 archaic retroposon insertions. We show that rheas are sister to the kiwis, emu and cassowaries, and confirm ratite paraphyly because tinamous are sister to moas. Divergence dating using 10 genes with broader taxon sampling, including emu, cassowary, ostrich, five kiwis, two rheas, three tinamous, three extinct moas and 15 neognath lineages, suggests that three vicariant events and possibly two dispersals are required to explain their historical biogeography. The age of crown group birds was estimated at 131 Ma (95% highest posterior density 122–138 Ma), similar to previous molecular estimates. Problems associated with gene tree discordance and incomplete lineage sorting in birds will require much larger gene sets to increase species tree accuracy and improve error in divergence times. The relatively rapid branching within neoaves pre-dates the extinction of dinosaurs, suggesting that the genesis of the radiation within this diverse clade of birds was not in response to the Cretaceous–Paleogene extinction event.

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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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Disentangling Sources of Gene Tree Discordance in Phylogenomic Data Sets: Testing Ancient Hybridizations in Amaranthaceae s.l

Systematic Biology ◽

10.1093/sysbio/syaa066 ◽

2020 ◽

Cited By ~ 1

Author(s):

Diego F Morales-Briones ◽

Gudrun Kadereit ◽

Delphine T Tefarikis ◽

Michael J Moore ◽

Stephen A Smith ◽

...

Keyword(s):

Network Inference ◽

Incomplete Lineage Sorting ◽

Gene Tree ◽

Phylogenetic Network ◽

Species Tree ◽

Data Sets ◽

Species Trees ◽

Lineage Sorting ◽

Data Set ◽

Gene Tree Discordance

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.]

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Phylogenomics Reveals Ancient Gene Tree Discordance in the Amphibian Tree of Life

Systematic Biology ◽

10.1093/sysbio/syaa034 ◽

2020 ◽

Vol 70 (1) ◽

pp. 49-66 ◽

Cited By ~ 4

Author(s):

Paul M Hime ◽

Alan R Lemmon ◽

Emily C Moriarty Lemmon ◽

Elizabeth Prendini ◽

Jeremy M Brown ◽

...

Keyword(s):

Tree Species ◽

Incomplete Lineage Sorting ◽

Phylogenetic Signal ◽

Gene Tree ◽

Strong Support ◽

Species Tree ◽

Tree Of Life ◽

Lineage Sorting ◽

Sister Relationship ◽

Gene Tree Discordance

Abstract Molecular phylogenies have yielded strong support for many parts of the amphibian Tree of Life, but poor support for the resolution of deeper nodes, including relationships among families and orders. To clarify these relationships, we provide a phylogenomic perspective on amphibian relationships by developing a taxon-specific Anchored Hybrid Enrichment protocol targeting hundreds of conserved exons which are effective across the class. After obtaining data from 220 loci for 286 species (representing 94% of the families and 44% of the genera), we estimate a phylogeny for extant amphibians and identify gene tree–species tree conflict across the deepest branches of the amphibian phylogeny. We perform locus-by-locus genealogical interrogation of alternative topological hypotheses for amphibian monophyly, focusing on interordinal relationships. We find that phylogenetic signal deep in the amphibian phylogeny varies greatly across loci in a manner that is consistent with incomplete lineage sorting in the ancestral lineage of extant amphibians. Our results overwhelmingly support amphibian monophyly and a sister relationship between frogs and salamanders, consistent with the Batrachia hypothesis. Species tree analyses converge on a small set of topological hypotheses for the relationships among extant amphibian families. These results clarify several contentious portions of the amphibian Tree of Life, which in conjunction with a set of vetted fossil calibrations, support a surprisingly younger timescale for crown and ordinal amphibian diversification than previously reported. More broadly, our study provides insight into the sources, magnitudes, and heterogeneity of support across loci in phylogenomic data sets.[AIC; Amphibia; Batrachia; Phylogeny; gene tree–species tree discordance; genomics; information theory.]

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Gene tree discordance causes apparent substitution rate variation

10.1101/029371 ◽

2015 ◽

Cited By ~ 1

Author(s):

Fabio K. Mendes ◽

Matthew W. Hahn

Keyword(s):

Substitution Rate ◽

Incomplete Lineage Sorting ◽

False Positive Rate ◽

Gene Tree ◽

Species Tree ◽

Rate Variation ◽

Species Trees ◽

Lineage Sorting ◽

Gene Tree Discordance ◽

Substitution Rate Variation

Substitution rates are known to be variable among genes, chromosomes, species, and lineages due to multifarious biological processes. Here we consider another source of substitution rate variation due to a technical bias associated with gene tree discordance, which has been found to be rampant in genome-wide datasets, often due to incomplete lineage sorting (ILS). This apparent substitution rate variation is caused when substitutions that occur on discordant gene trees are analyzed in the context of a single, fixed species tree. Such substitutions have to be resolved by proposing multiple substitutions on the species tree, and we therefore refer to this phenomenon as "SPILS" (Substitutions Produced by Incomplete Lineage Sorting). We use simulations to demonstrate that SPILS has a larger effect with increasing levels of ILS, and on trees with larger numbers of taxa. Specific branches of the species trees are consistently, but erroneously, inferred to be longer or shorter, and we show that these branches can be predicted based on discordant tree topologies. Moreover, we observe that fixing a species tree topology when performing tests of positive selection increases the false positive rate, particularly for genes whose discordant topologies are most affected by SPILS. Finally, we use data from multipleDrosophilaspecies to show that SPILS can be detected in nature. While the effects of SPILS are modest per gene, it has the potential to affect substitution rate variation whenever high levels of ILS are present, particularly in rapid radiations. The problems outlined here have implications for character mapping of any type of trait, and for any biological process that causes discordance. We discuss possible solutions to these problems, and areas in which they are likely to have caused faulty inferences of convergence and accelerated evolution.

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

Systematic Biology ◽

10.1093/sysbio/syaa083 ◽

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.

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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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Dissecting the basis of novel trait evolution in a radiation with widespread phylogenetic discordance

10.1101/201376 ◽

2017 ◽

Cited By ~ 3

Author(s):

Meng Wu ◽

Jamie L. Kostyun ◽

Matthew W. Hahn ◽

Leonie Moyle

Keyword(s):

De Novo ◽

Incomplete Lineage Sorting ◽

Phylogenetic Analyses ◽

Gene Tree ◽

Fruit Color ◽

Species Tree ◽

Color Variation ◽

Lineage Sorting ◽

Floral Character ◽

Trait Evolution

ABSTRACTPhylogenetic analyses of trait evolution can provide insight into the evolutionary processes that initiate and drive phenotypic diversification. However, recent phylogenomic studies have revealed extensive gene tree-species tree discordance, which can lead to incorrect inferences of trait evolution if only a single species tree is used for analysis. This phenomenon—dubbed “hemiplasy”—is particularly important to consider during analyses of character evolution in rapidly radiating groups, where discordance is widespread. Here we generate whole-transcriptome data for a phylogenetic analysis of 14 species in the plant genus Jaltomata (the sister clade to Solanum), which has experienced rapid, recent trait evolution, including in fruit and nectar color, and flower size and shape. Consistent with other radiations, we find evidence for rampant gene tree discordance due to incomplete lineage sorting (ILS) and several introgression events among the well-supported subclades. Since both ILS and introgression increase the probability of hemiplasy, we perform several analyses that take discordance into account while identifying genes that might contribute to phenotypic evolution. Despite discordance, the history of fruit color evolution in Jaltomata can be inferred with high confidence, and we find evidence of de novo adaptive evolution at individual genes associated with fruit color variation. In contrast, hemiplasy appears to strongly affect inferences about floral character transitions in Jaltomata, and we identify candidate loci that could arise either from multiple lineage-specific substitutions or standing ancestral polymorphisms. Our analysis provides a generalizable example of how to manage discordance when identifying loci associated with trait evolution in a radiating lineage.

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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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Sage Insights Into the Phylogeny of Salvia: Dealing With Sources of Discordance Within and Across Genomes

Frontiers in Plant Science ◽

10.3389/fpls.2021.767478 ◽

2021 ◽

Vol 12 ◽

Author(s):

Jeffrey P. Rose ◽

Ricardo Kriebel ◽

Larissa Kahan ◽

Alexa DiNicola ◽

Jesús G. González-Gallegos ◽

...

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Divergence Time ◽

Time Estimation ◽

Single Copy ◽

Lineage Sorting ◽

Divergence Time Estimation ◽

Sequencing Technologies ◽

Plastid Genomes ◽

Gene Tree Discordance

Next-generation sequencing technologies have facilitated new phylogenomic approaches to help clarify previously intractable relationships while simultaneously highlighting the pervasive nature of incongruence within and among genomes that can complicate definitive taxonomic conclusions. Salvia L., with ∼1,000 species, makes up nearly 15% of the species diversity in the mint family and has attracted great interest from biologists across subdisciplines. Despite the great progress that has been achieved in discerning the placement of Salvia within Lamiaceae and in clarifying its infrageneric relationships through plastid, nuclear ribosomal, and nuclear single-copy genes, the incomplete resolution has left open major questions regarding the phylogenetic relationships among and within the subgenera, as well as to what extent the infrageneric relationships differ across genomes. We expanded a previously published anchored hybrid enrichment dataset of 35 exemplars of Salvia to 179 terminals. We also reconstructed nearly complete plastomes for these samples from off-target reads. We used these data to examine the concordance and discordance among the nuclear loci and between the nuclear and plastid genomes in detail, elucidating both broad-scale and species-level relationships within Salvia. We found that despite the widespread gene tree discordance, nuclear phylogenies reconstructed using concatenated, coalescent, and network-based approaches recover a common backbone topology. Moreover, all subgenera, except for Audibertia, are strongly supported as monophyletic in all analyses. The plastome genealogy is largely resolved and is congruent with the nuclear backbone. However, multiple analyses suggest that incomplete lineage sorting does not fully explain the gene tree discordance. Instead, horizontal gene flow has been important in both the deep and more recent history of Salvia. Our results provide a robust species tree of Salvia across phylogenetic scales and genomes. Future comparative analyses in the genus will need to account for the impacts of hybridization/introgression and incomplete lineage sorting in topology and divergence time estimation.

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