Phylogenomic analyses of Alternaria section Alternaria: A high-resolution, genome-wide study of lineage sorting and gene tree discordance

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.

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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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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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Gene tree discordance generates patterns of diminishing convergence over time

10.1101/059006 ◽

2016 ◽

Cited By ~ 1

Author(s):

Fabio K. Mendes ◽

Yoonsoo Hahn ◽

Matthew W. Hahn

Keyword(s):

Gene Tree ◽

Primate Species ◽

Epistatic Interactions ◽

Genome Wide ◽

Tree Inference ◽

Gene Tree Discordance ◽

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

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2012.1630 ◽

2012 ◽

Vol 279 (1747) ◽

pp. 4617-4625 ◽

Cited By ~ 66

Author(s):

Oliver Haddrath ◽

Allan J. Baker

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Species Tree ◽

Nuclear Genes ◽

Lineage Sorting ◽

Posterior Density ◽

Crown Group ◽

Gene Sets ◽

Gene Tree Discordance ◽

Highest Posterior Density

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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Widespread paleopolyploidy, gene tree conflict, and recalcitrant relationships among the carnivorous Caryophyllales

10.1101/115741 ◽

2017 ◽

Cited By ~ 1

Author(s):

Joseph F. Walker ◽

Ya Yang ◽

Michael J. Moore ◽

Jessica Mikenas ◽

Alfonso Timoneda ◽

...

Keyword(s):

Gene Tree ◽

West African ◽

Evolutionary Relationships ◽

Taxon Sampling ◽

Data Sets ◽

List Type ◽

Data Set ◽

Present Evidence ◽

Gene Tree Discordance ◽

Phylogenomic Analyses

ABSTRACTThe carnivorous members of the large, hyperdiverse Caryophyllales (e.g. Venus flytrap, sundews and Nepenthes pitcher plants) represent perhaps the oldest and most diverse lineage of carnivorous plants. However, despite numerous studies seeking to elucidate their evolutionary relationships, the early-diverging relationships remain unresolved.To explore the utility of phylogenomic data sets for resolving relationships among the carnivorous Caryophyllales, we sequenced ten transcriptomes, including all the carnivorous genera except those in the rare West African liana family (Dioncophyllaceae). We used a variety of methods to infer the species tree, examine gene tree conflict and infer paleopolyploidy events.Phylogenomic analyses support the monophyly of the carnivorous Caryophyllales, with an origin of 68-83 mya. In contrast to previous analyses recover the remaining non-core Caryophyllales as non-monophyletic, although there are multiple reasons this result may be spurious and node supporting this relationship contains a significant amount gene tree discordance. We present evidence that the clade contains at least seven independent paleopolyploidy events, previously debated nodes from the literature have high levels of gene tree conflict, and taxon sampling influences topology even in a phylogenomic data set.Our data demonstrate the importance of carefully considering gene tree conflict and taxon sampling in phylogenomic analyses. Moreover, they provide a remarkable example of the propensity for paleopolyploidy in angiosperms, with at least seven such events in a clade of less than 2500 species.

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Introgression across evolutionary scales suggests reticulation contributes to Amazonian tree diversity

10.1101/2019.12.12.873927 ◽

2019 ◽

Author(s):

Rowan J. Schley ◽

R. Toby Pennington ◽

Oscar Alejandro Pérez-Escobar ◽

Andrew J. Helmstetter ◽

Manuel de la Estrella ◽

...

Keyword(s):

Gene Flow ◽

Incomplete Lineage Sorting ◽

Gene Tree ◽

Reticulate Evolution ◽

Specific Gene ◽

Lineage Sorting ◽

Closely Related Species ◽

Genome Wide ◽

High Degree ◽

Prevailing View

AbstractHybridization has the potential to generate or homogenize biodiversity and is a particularly common phenomenon in plants, with an estimated 25% of species undergoing inter-specific gene flow. However, hybridization in Amazonia’s megadiverse tree flora was assumed to be extremely rare despite extensive sympatry between closely related species, and its role in diversification remains enigmatic because it has not yet been examined empirically. Using members of a dominant Amazonian tree family (Brownea, Fabaceae) as a model to address this knowledge gap, our study recovered extensive evidence of hybridization among multiple lineages across phylogenetic scales. More specifically, our results uncovered several historical introgression events between Brownea lineages and indicated that gene tree incongruence in Brownea is best explained by introgression, rather than solely by incomplete lineage sorting. Furthermore, investigation of recent hybridization using ∼19,000 ddRAD loci recovered a high degree of shared variation between two Brownea species which co-occur in the Ecuadorian Amazon. Our analyses also showed that these sympatric lineages exhibit homogeneous rates of introgression among loci relative to the genome-wide average, implying a lack of selection against hybrid genotypes and a persistence of hybridization over time. Our results demonstrate that gene flow between multiple Amazonian tree species has occurred across temporal scales, and contrasts with the prevailing view of hybridization’s rarity in Amazonia. Overall, our results provide novel evidence that reticulate evolution influenced diversification in part of the Amazonian tree flora, which is the most diverse on Earth.

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

10.1101/2021.03.25.436973 ◽

2021 ◽

Author(s):

Edeline Gagnon ◽

Rebecca Hilgenhof ◽

Andr&eacutes Orejuela ◽

Angela McDonnell ◽

Gaurav Sablok ◽

...

Keyword(s):

Phylogenetic Trees ◽

Incomplete Lineage Sorting ◽

Gene Tree ◽

Flowering Plant ◽

Gene Trees ◽

Species Trees ◽

Nuclear Target ◽

Lineage Sorting ◽

Target Capture ◽

Gene Tree Discordance

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.

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