Bears in a Forest of Gene Trees: Phylogenetic Inference Is Complicated by Incomplete Lineage Sorting and Gene Flow

AbstractThe multispecies network coalescent (MSNC) is a stochastic process that captures how gene trees grow within the branches of a phylogenetic network. Coupling the MSNC with a stochastic mutational process that operates along the branches of the gene trees gives rise to a generative model of how multiple loci from within and across species evolve in the presence of both incomplete lineage sorting (ILS) and reticulation (e.g., hybridization). We report on a Bayesian method for sampling the parameters of this generative model, including the species phylogeny, gene trees, divergence times, and population sizes, from DNA sequences of multiple independent loci. We demonstrate the utility of our method by analyzing simulated data and reanalyzing three biological data sets. Our results demonstrate the significance of not only co-estimating species phylogenies and gene trees, but also accounting for reticulation and ILS simultaneously. In particular, we show that when gene flow occurs, our method accurately estimates the evolutionary histories, coalescence times, and divergence times. Tree inference methods, on the other hand, underestimate divergence times and overestimate coalescence times when the evolutionary history is reticulate. While the MSNC corresponds to an abstract model of “intermixture,” we study the performance of the model and method on simulated data generated under a gene flow model. We show that the method accurately infers the most recent time at which gene flow occurs. Finally, we demonstrate the application of the new method to a 106-locus yeast data set. [Multispecies network coalescent; reticulation; incomplete lineage sorting; phylogenetic network; Bayesian inference; RJMCMC.]

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The genomic view of diversification

10.1101/413427 ◽

2018 ◽

Author(s):

Julie Marin ◽

Guillaume Achaz ◽

Anton Crombach ◽

Amaury Lambert

Keyword(s):

Gene Flow ◽

Incomplete Lineage Sorting ◽

Molecular Data ◽

Species Tree ◽

Data Sets ◽

Gene Trees ◽

Lineage Sorting ◽

Parameters Tuning ◽

History Of ◽

New Framework

AbstractEvolutionary relationships between species are traditionally represented in the form of a tree, the species tree. Its reconstruction from molecular data is hindered by frequent conflicts between gene genealogies. Usually, these disagreements are explained by incomplete lineage sorting (ILS) due to random coalescences of gene lineages inside the edges of the species tree. This paradigm, the multi-species coalescent (MSC), is constantly violated by the ubiquitous presence of gene flow, leading to incongruences between gene trees that cannot be explained by ILS alone. Here we argue instead in favor of a vision acknowledging the importance of gene flow and where gene histories shape the species tree rather than the opposite. We propose a new framework for modeling the joint evolution of gene and species lineages relaxing the hierarchy between the species tree and gene trees. We implement this framework in two mathematical models called the gene-based diversification models (GBD): 1) GBD-forward following all evolving genomes and 2) GBD-backward based on coalescent theory. They feature four parameters tuning colonization, gene flow, genetic drift and genetic differentiation. We propose a quick inference method based on differences between gene trees. Applied to two empirical data-sets prone to gene flow, we find a better support for the GBD model than for the MSC model. Along with the increasing awareness of the extent of gene flow, this work shows the importance of considering the richer signal contained in genomic histories, rather than in the mere species tree, to better apprehend the complex evolutionary history of species.

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Speciation genes are more likely to have discordant gene trees

10.1101/244822 ◽

2018 ◽

Cited By ~ 1

Author(s):

Richard J. Wang ◽

Matthew W. Hahn

Keyword(s):

Gene Flow ◽

Reproductive Isolation ◽

Incomplete Lineage Sorting ◽

Gene Trees ◽

Species Trees ◽

Species Relationships ◽

Lineage Sorting ◽

Epistatic Interactions ◽

Speciation Event ◽

History Of

AbstractSpeciation genes are responsible for reproductive isolation between species. By directly participating in the process of speciation, the genealogies of isolating loci have been thought to more faithfully represent species trees. The unique properties of speciation genes may provide valuable evolutionary insights and help determine the true history of species divergence. Here, we formally analyze whether genealogies from loci participating in Dobzhansky-Muller (DM) incompatibilities are more likely to be concordant with the species tree under incomplete lineage sorting (ILS). Individual loci differ stochastically from the true history of divergence with a predictable frequency due to ILS, and these expectations—combined with the DM model of intrinsic reproductive isolation from epistatic interactions—can be used to examine the probability of concordance at isolating loci. Contrary to existing verbal models, we find that reproductively isolating loci that follow the DM model are often more likely to have discordant gene trees. These results are dependent on the pattern of isolation observed between three species, the time between speciation events, and the time since the last speciation event. Results supporting a higher probability of discordance are found for both derived-derived and derived-ancestral DM pairs, and regardless of whether incompatibilities are allowed or prohibited from segregating in the same population. Our overall results suggest that DM loci are unlikely to be especially useful for reconstructing species relationships, even in the presence of gene flow between incipient species, and may in fact be positively misleading.

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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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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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Shallow genetic divergence and distinct phenotypic differences between two Andean hummingbirds: Speciation with gene flow?

The Auk ◽

10.1093/auk/ukz046 ◽

2019 ◽

Vol 136 (4) ◽

Cited By ~ 3

Author(s):

Catalina Palacios ◽

Silvana García-R ◽

Juan Luis Parra ◽

Andrés M Cuervo ◽

F Gary Stiles ◽

...

Keyword(s):

Gene Flow ◽

Genetic Differentiation ◽

Incomplete Lineage Sorting ◽

Lineage Sorting ◽

Phenotypic Differences ◽

Adaptive Mechanisms ◽

The Face ◽

Gloger’S Rule ◽

Divergence With Gene Flow ◽

Neutral Markers

Abstract Ecological speciation can proceed despite genetic interchange when selection counteracts the homogenizing effects of migration. We tested predictions of this divergence-with-gene-flow model in Coeligena helianthea and C. bonapartei, 2 parapatric Andean hummingbirds with marked plumage divergence. We sequenced putatively neutral markers (mitochondrial DNA [mtDNA] and nuclear ultraconserved elements [UCEs]) to examine genetic structure and gene flow, and a candidate gene (MC1R) to assess its role underlying divergence in coloration. We also tested the prediction of Gloger’s rule that darker forms occur in more humid environments, and examined morphological variation to assess adaptive mechanisms potentially promoting divergence. Genetic differentiation between species was low in both ND2 and UCEs. Coalescent estimates of migration were consistent with divergence with gene flow, but we cannot reject incomplete lineage sorting reflecting recent speciation as an explanation for patterns of genetic variation. MC1R variation was unrelated to phenotypic differences. Species did not differ in macroclimatic niches but were distinct in morphology. Although we reject adaptation to variation in macroclimatic conditions as a cause of divergence, speciation may have occurred in the face of gene flow driven by other ecological pressures or by sexual selection. Marked phenotypic divergence with no neutral genetic differentiation is remarkable for Neotropical birds, and makes C. helianthea and C. bonapartei an appropriate system in which to search for the genetic basis of species differences employing genomics.

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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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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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