Determining the probability of hemiplasy in the presence of incomplete lineage sorting and introgression

The incongruence of character states with phylogenetic relationships is often interpreted as evidence of convergent evolution. However, trait evolution along discordant gene trees can also generate these incongruences – a phenomenon known as hemiplasy. Classic comparative methods do not account for discordance, resulting in incorrect inferences about the number, timing, and direction of trait transitions. Biological sources of discordance include incomplete lineage sorting (ILS) and introgression, but only ILS has received theoretical consideration in the context of hemiplasy. Here, we present a model that shows introgression makes hemiplasy more likely, such that methods that account for ILS alone will be conservative. We also present a method and software (HeIST) for making statistical inferences about the probability of hemiplasy and homoplasy in large datasets that contain both ILS and introgression. We apply our methods to two empirical datasets, finding that hemiplasy is likely to contribute to the observed trait incongruences in both.

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Determining the probability of hemiplasy in the presence of incomplete lineage sorting and introgression

10.1101/2020.04.15.043752 ◽

2020 ◽

Cited By ~ 2

Author(s):

Mark S. Hibbins ◽

Matthew J.S. Gibson ◽

Matthew W. Hahn

Keyword(s):

Software Package ◽

Incomplete Lineage Sorting ◽

Most Probable Number ◽

Phylogenetic Comparative Methods ◽

Simulation Tool ◽

Gene Trees ◽

Lineage Sorting ◽

Probable Number ◽

Statistical Inferences ◽

Biological Sources

AbstractThe incongruence of character states with phylogenetic relationships is often interpreted as evidence of convergent evolution. However, trait evolution along discordant gene trees can also generate these incongruences – a phenomenon known as hemiplasy. Classic phylogenetic comparative methods do not account for discordance, resulting in incorrect inferences about the number of times a trait has evolved, and therefore about convergence. Biological sources of discordance include incomplete lineage sorting (ILS) and introgression, but only ILS has received theoretical consideration in the context of hemiplasy. Here, we derive expectations for the probabilities of hemiplasy and homoplasy with ILS and introgression acting simultaneously. We find that introgression makes hemiplasy more likely than ILS alone, suggesting that methods that account for discordance only due to ILS will be conservative. We also present a method for making statistical inferences about the relative probabilities of hemiplasy and homoplasy in empirical datasets. Our method is implemented in the software package HeIST (Hemiplasy Inference Simulation Tool), and estimates the most probable number of transitions among character states given a set of relationships with discordance. HeIST can accommodate ILS and introgression simultaneously, and can be applied to phylogenies where the number of taxa makes finding an analytical solution impractical. We apply this tool to two empirical cases of apparent trait convergence in the presence of high levels of discordance, one of which involves introgression between the convergent lineages. In both cases we find that hemiplasy is likely to contribute to the observed trait incongruences.

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Deciphering phylogenetic relationships and delimiting species boundaries using a Bayesian coalescent approach in protists: A case study of the ciliate genus Spirostomum (Ciliophora, Heterotrichea)

Scientific Reports ◽

10.1038/s41598-019-52722-4 ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 6

Author(s):

Shahed Uddin Ahmed Shazib ◽

Peter Vďačný ◽

Marek Slovák ◽

Eleni Gentekaki ◽

Mann Kyoon Shin

Keyword(s):

Phylogenetic Relationships ◽

Incomplete Lineage Sorting ◽

Molecular Data ◽

Species Boundaries ◽

Gene Trees ◽

Lineage Sorting ◽

Alpha Tubulin ◽

Individual Gene ◽

Coalescent Approach ◽

Analytical Approaches

Abstract The ciliate genus Spirostomum comprises eight morphospecies, inhabiting diverse aquatic environments worldwide, where they can be used as water quality indicators. Although Spirostomum species are relatively easily identified using morphological methods, the previous nuclear rDNA-based phylogenies indicated several conflicts in morphospecies delineation. Moreover, the single locus phylogenies and previous analytical approaches could not unambiguously resolve phylogenetic relationships among Spirostomum morphospecies. Here, we attempt to investigate species boundaries and evolutionary history of Spirostomum taxa, using 166 new sequences from multiple populations employing one mitochondrial locus (CO1 gene) and two nuclear loci (rRNA operon and alpha-tubulin gene). In accordance with previous studies, relationships among the eight Spirostomum morphospecies were poorly supported statistically in individual gene trees. To overcome this problem, we utilised for the first time in ciliates the Bayesian coalescent approach, which accounts for ancestral polymorphisms, incomplete lineage sorting, and recombination. This strategy enabled us to robustly resolve deep relationships between Spirostomum species and to support the hypothesis that taxa with compact macronucleus and taxa with moniliform macronucleus each form a distinct lineage. Bayesian coalescent-based delimitation analyses strongly statistically supported the traditional morphospecies concept but also indicated that there are two S. minus-like cryptic species and S. teres is non-monophyletic. Spirostomum teres was very likely defined by a set of ancestral features of lineages that also gave rise to S. yagiui and S. dharwarensis. However, molecular data from type populations of the morphospecies S. minus and S. teres are required to unambiguously resolve the taxonomic problems.

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Faculty Opinions recommendation of Widespread discordance of gene trees with species tree in Drosophila: evidence for incomplete lineage sorting.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1052717.504629 ◽

2006 ◽

Author(s):

Artyom Kopp

Keyword(s):

Incomplete Lineage Sorting ◽

Species Tree ◽

Gene Trees ◽

Lineage Sorting

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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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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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Detecting destabilizing species in the phylogenetic backbone of Potentilla (Rosaceae) using low-copy nuclear markers

AoB Plants ◽

10.1093/aobpla/plaa017 ◽

2020 ◽

Vol 12 (3) ◽

Cited By ~ 1

Author(s):

Nannie L Persson ◽

Ingrid Toresen ◽

Heidi Lie Andersen ◽

Jenny E E Smedmark ◽

Torsten Eriksson

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Data Sets ◽

Gene Trees ◽

Lineage Sorting ◽

Nuclear Markers ◽

Data Set ◽

Multispecies Coalescent ◽

Single Marker ◽

Named Groups

Abstract The genus Potentilla (Rosaceae) has been subjected to several phylogenetic studies, but resolving its evolutionary history has proven challenging. Previous analyses recovered six, informally named, groups: the Argentea, Ivesioid, Fragarioides, Reptans, Alba and Anserina clades, but the relationships among some of these clades differ between data sets. The Reptans clade, which includes the type species of Potentilla, has been noticed to shift position between plastid and nuclear ribosomal data sets. We studied this incongruence by analysing four low-copy nuclear markers, in addition to chloroplast and nuclear ribosomal data, with a set of Bayesian phylogenetic and Multispecies Coalescent (MSC) analyses. A selective taxon removal strategy demonstrated that the included representatives from the Fragarioides clade, P. dickinsii and P. fragarioides, were the main sources of the instability seen in the trees. The Fragarioides species showed different relationships in each gene tree, and were only supported as a monophyletic group in a single marker when the Reptans clade was excluded from the analysis. The incongruences could not be explained by allopolyploidy, but rather by homoploid hybridization, incomplete lineage sorting or taxon sampling effects. When P. dickinsii and P. fragarioides were removed from the data set, a fully resolved, supported backbone phylogeny of Potentilla was obtained in the MSC analysis. Additionally, indications of autopolyploid origins of the Reptans and Ivesioid clades were discovered in the low-copy gene trees.

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Phylogenetic relationships based on nuclear and plastid DNA sequences reveal recent diversification and discordant patterns of morphological evolution of the Chilean genera of Gilliesieae (Amaryllidaceae: Allioideae)

Botanical Journal of the Linnean Society ◽

10.1093/botlinnean/boaa035 ◽

2020 ◽

Vol 194 (1) ◽

pp. 84-99

Author(s):

Inelia Escobar ◽

Eduardo Ruiz-Ponce ◽

Paula J Rudall ◽

Michael F Fay ◽

Oscar Toro-Núñez ◽

...

Keyword(s):

Dna Sequences ◽

Phylogenetic Relationships ◽

Incomplete Lineage Sorting ◽

Morphological Evolution ◽

Strong Support ◽

Plastid Dna ◽

Lineage Sorting ◽

Generic Level ◽

Molecular Analyses ◽

Floral Diversity

Abstract Gilliesieae are a South American tribe of Amaryllidaceae characterized by high floral diversity. Given different taxonomic interpretations and proposals for generic and specific relationships, a representative phylogenetic analysis is required to clarify the systematics of this group. The present study provides a framework for understanding phylogenetic relationships and contributing to the development of an appropriate taxonomic treatment of Gilliesieae. Molecular analyses, based on nuclear (ITS) and plastid DNA sequences (trnL-F and rbcL), resolve with strong support the monophyly of the tribe and the differentiation of two major clades. Clade I comprises the genera Gilliesia, Gethyum and Solaria and Clade II includes Miersia and Speea. These well-supported clades are mostly congruent with vegetative and karyotype characters rather than, e.g., floral symmetry. At the generic level, all molecular analyses reveal the paraphyly of Gilliesia and Miersia. Gethyum was found to be paraphyletic, resulting in the confirmation of Ancrumia as a distinct genus. Several instances of incongruent phylogenetic signals were found among data sets. The calibrated tree suggests a recent diversification of the tribe (Pliocene–Pleistocene), a contemporary process of speciation in which instances of hybridization and incomplete lineage sorting could explain patterns of paraphyly and incongruence of floral morphology.

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Multilocus phylogeny of Gryllus field crickets (Orthoptera: Gryllidae: Gryllinae) utilizing anchored hybrid enrichment

Zootaxa ◽

10.11646/zootaxa.4750.3.2 ◽

2020 ◽

Vol 4750 (3) ◽

pp. 328-348 ◽

Cited By ~ 2

Author(s):

DAVID A. GRAY ◽

DAVID B. WEISSMAN ◽

JEFFREY A. COLE ◽

EMILY MORIARTY LEMMON

Keyword(s):

Sequence Data ◽

Incomplete Lineage Sorting ◽

The United States ◽

Field Cricket ◽

Future Research ◽

Gene Trees ◽

Lineage Sorting ◽

The Bahamas ◽

Field Crickets ◽

Anchored Hybrid Enrichment

We present the first comprehensive molecular phylogeny of Gryllus field cricket species found in the United States and Canada, select additional named Gryllus species found in Mexico and the Bahamas, plus the European field cricket G. campestris Linnaeus and the Afro-Eurasian cricket G. bimaculatus De Geer. Acheta, Teleogryllus, and Nigrogryllus were used as outgroups. Anchored hybrid enrichment was used to generate 492,531 base pairs of DNA sequence from 563 loci. RAxML analysis of concatenated sequence data and Astral analysis of gene trees gave broadly congruent results, especially for older branches and overall tree structure. The North American Gryllus are monophyletic with respect to the two Old World taxa; certain sub-groups show rapid recent divergence. This is the first Anchored Hybrid Enrichment study of an insect group done for closely related species within a single genus, and the results illustrate the challenges of reconstructing the evolutionary history of young rapidly diverged taxa when both incomplete lineage sorting and probable hybridization are at play. Because Gryllus field crickets have been used extensively as a model system in evolutionary ecology, behavior, neuro-physiology, speciation, and life-history and life-cycle evolution, these results will help inform, interpret, and guide future research in these areas.

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