Introgression across evolutionary scales suggests reticulation contributes to Amazonian tree diversity

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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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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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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Target enrichment improves phylogenetic resolution in the genus Zanthoxylum (Rutaceae) and indicates both incomplete lineage sorting and hybridization events

10.1101/2021.04.12.439519 ◽

2021 ◽

Author(s):

Niklas Reichelt ◽

Jun Wen ◽

Claudia Paetzold ◽

Marc Appelhans

Keyword(s):

High Throughput Sequencing ◽

Incomplete Lineage Sorting ◽

Phylogenetic Analyses ◽

Gene Tree ◽

Single Copy ◽

Reticulate Evolution ◽

Gene Trees ◽

Target Enrichment ◽

Lineage Sorting ◽

Phylogenetic Resolution

Background and aims: Zanthoxylum L. is the only pantropical genus within Rutaceae, with a few species native to temperate eastern Asia and North America. Efforts using Sanger sequencing failed to resolve the backbone phylogeny of Zanthoxylum. In this study, we employed target enrichment high-throughput sequencing to improve resolution. Gene trees were examined for concordance and sectional classifications of Zanthoxylum were evaluated. Off-target reads were investigated to identify putative single-copy markers for bait refinement, and low-copy markers for evidence of putative hybridization events. Methods: We developed a custom bait set for target enrichment of 745 exons in Zanthoxylum and applied it to 45 Zanthoxylum species and one Tetradium species as the outgroup. Illumina reads were processed via the HybPhyloMaker pipeline. Phylogenetic inferences were conducted using coalescent and concatenated methods. Concordance was assessed using quartet sampling. Off-target reads were assembled and putative single- and low-copy genes were extracted. Additional phylogenetic analyses were performed based on these alignments. Key results: Four major clades are supported within Zanthoxylum: the African clade, the Z. asiaticum clade, the Asian-Pacific-Australian clade, and the American-eastern Asian clade. While overall support has improved, regions of conflict are similar to those previously observed. Gene tree discordances indicate a hybridization event in the ancestor of the Hawaiian lineage, and incomplete lineage sorting for the American backbone. Off-target putative single-copy genes largely confirm on-target results, and putative low-copy genes provide additional evidence for hybridization in the Hawaiian lineage. Only two of the five sections of Zanthoxylum are resolved as monophyletic. Conclusion: Target enrichment is suitable to assess phylogenetic relationships in Zanthoxylum. Our phylogenetic analyses reveal that current sectional classifications need revision. Quartet tree concordance indicates several instances of reticulate evolution. Off-target reads are proven useful to identify additional phylogenetically informative regions for bait refinement or gene tree based approaches.

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Extensive Genome-Wide Phylogenetic Discordance Is Due to Incomplete Lineage Sorting and Not Ongoing Introgression in a Rapidly Radiated Bryophyte Genus

Molecular Biology and Evolution ◽

10.1093/molbev/msab063 ◽

2021 ◽

Author(s):

Olena Meleshko ◽

Michael D Martin ◽

Thorfinn Sand Korneliussen ◽

Christian Schröck ◽

Paul Lamkowski ◽

...

Keyword(s):

Gene Flow ◽

Incomplete Lineage Sorting ◽

Nuclear Genome ◽

Lineage Sorting ◽

Rapid Radiation ◽

Organellar Genomes ◽

Genome Wide ◽

Phylogenetic Discordance ◽

Species Groups ◽

Open Question

Abstract The relative importance of introgression for diversification has long been a highly disputed topic in speciation research and remains an open question despite the great attention it has received over the past decade. Gene flow leaves traces in the genome similar to those created by incomplete lineage sorting (ILS), and identification and quantification of gene flow in the presence of ILS is challenging and requires knowledge about the true phylogenetic relationship among the species. We use whole nuclear, plastid, and organellar genomes from 12 species in the rapidly radiated, ecologically diverse, actively hybridizing genus of peatmoss (Sphagnum) to reconstruct the species phylogeny and quantify introgression using a suite of phylogenomic methods. We found extensive phylogenetic discordance among nuclear and organellar phylogenies, as well as across the nuclear genome and the nodes in the species tree, best explained by extensive ILS following the rapid radiation of the genus rather than by postspeciation introgression. Our analyses support the idea of ancient introgression among the ancestral lineages followed by ILS, whereas recent gene flow among the species is highly restricted despite widespread interspecific hybridization known in the group. Our results contribute to phylogenomic understanding of how speciation proceeds in rapidly radiated, actively hybridizing species groups, and demonstrate that employing a combination of diverse phylogenomic methods can facilitate untangling complex phylogenetic patterns created by ILS and introgression.

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Phylogenetic Trees and Networks Can Serve as Powerful and Complementary Approaches for Analysis of Genomic Data

Systematic Biology ◽

10.1093/sysbio/syz056 ◽

2019 ◽

Vol 69 (3) ◽

pp. 593-601 ◽

Cited By ~ 9

Author(s):

Christopher Blair ◽

Cécile Ané

Keyword(s):

Gene Flow ◽

Phylogenetic Trees ◽

Evolutionary History ◽

Incomplete Lineage Sorting ◽

Gene Tree ◽

Phylogenetic Network ◽

Genomic Data ◽

Point Of View ◽

Phylogenetic Networks ◽

Lineage Sorting

Abstract Genomic data have had a profound impact on nearly every biological discipline. In systematics and phylogenetics, the thousands of loci that are now being sequenced can be analyzed under the multispecies coalescent model (MSC) to explicitly account for gene tree discordance due to incomplete lineage sorting (ILS). However, the MSC assumes no gene flow post divergence, calling for additional methods that can accommodate this limitation. Explicit phylogenetic network methods have emerged, which can simultaneously account for ILS and gene flow by representing evolutionary history as a directed acyclic graph. In this point of view, we highlight some of the strengths and limitations of phylogenetic networks and argue that tree-based inference should not be blindly abandoned in favor of networks simply because they represent more parameter rich models. Attention should be given to model selection of reticulation complexity, and the most robust conclusions regarding evolutionary history are likely obtained when combining tree- and network-based inference.

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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

10.1101/2020.05.26.112318 ◽

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

ABSTRACTThe 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 alone includes nine of the top ten most unstable nodes in angiosperms, and the recalcitrant relationships along the backbone of the order 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 15%, 52%, and 32% 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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Out of Sight, Out of Mind: Widespread Nuclear and Plastid-Nuclear Discordance in the Flowering Plant Genus Polemonium (Polemoniaceae) Suggests Widespread Historical Gene Flow Despite Limited Nuclear Signal

Systematic Biology ◽

10.1093/sysbio/syaa049 ◽

2020 ◽

Vol 70 (1) ◽

pp. 162-180

Author(s):

Jeffrey P Rose ◽

Cassio A P Toledo ◽

Emily Moriarty Lemmon ◽

Alan R Lemmon ◽

Kenneth J Sytsma

Keyword(s):

Gene Flow ◽

Evolutionary History ◽

Plastid Genome ◽

Incomplete Lineage Sorting ◽

Nuclear Genome ◽

Reticulate Evolution ◽

Phylogenetic Networks ◽

Flowering Plant ◽

Lineage Sorting ◽

History Of

Abstract Phylogenomic data from a rapidly increasing number of studies provide new evidence for resolving relationships in recently radiated clades, but they also pose new challenges for inferring evolutionary histories. Most existing methods for reconstructing phylogenetic hypotheses rely solely on algorithms that only consider incomplete lineage sorting (ILS) as a cause of intra- or intergenomic discordance. Here, we utilize a variety of methods, including those to infer phylogenetic networks, to account for both ILS and introgression as a cause for nuclear and cytoplasmic-nuclear discordance using phylogenomic data from the recently radiated flowering plant genus Polemonium (Polemoniaceae), an ecologically diverse genus in Western North America with known and suspected gene flow between species. We find evidence for widespread discordance among nuclear loci that can be explained by both ILS and reticulate evolution in the evolutionary history of Polemonium. Furthermore, the histories of organellar genomes show strong discordance with the inferred species tree from the nuclear genome. Discordance between the nuclear and plastid genome is not completely explained by ILS, and only one case of discordance is explained by detected introgression events. Our results suggest that multiple processes have been involved in the evolutionary history of Polemonium and that the plastid genome does not accurately reflect species relationships. We discuss several potential causes for this cytoplasmic-nuclear discordance, which emerging evidence suggests is more widespread across the Tree of Life than previously thought. [Cyto-nuclear discordance, genomic discordance, phylogenetic networks, plastid capture, Polemoniaceae, Polemonium, reticulations.]

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Molecular Signatures of Reticulate Evolution within the Complex of European Pine Taxa

Forests ◽

10.3390/f12040489 ◽

2021 ◽

Vol 12 (4) ◽

pp. 489

Author(s):

Bartosz Łabiszak ◽

Witold Wachowiak

Keyword(s):

Gene Flow ◽

Reticulate Evolution ◽

Modeling Framework ◽

Closely Related Species ◽

Interspecific Gene Flow ◽

Nucleotide Sequence Variation ◽

History Of ◽

Best Fitting ◽

Species Integrity

Speciation mechanisms, including the role of interspecific gene flow and introgression in the emergence of new species, are the major focus of evolutionary studies. Inference of taxonomic relationship between closely related species may be challenged by past hybridization events, but at the same time, it may provide new knowledge about mechanisms responsible for the maintenance of species integrity despite interspecific gene flow. Here, using nucleotide sequence variation and utilizing a coalescent modeling framework, we tested the role of hybridization and introgression in the evolutionary history of closely related pine taxa from the Pinus mugo complex and P. sylvestris. We compared the patterns of polymorphism and divergence between taxa and found a great overlap of neutral variation within the P. mugo complex. Our phylogeny reconstruction indicated multiple instances of reticulation events in the past, suggesting an important role of interspecific gene flow in the species divergence. The best-fitting model revealed P. mugo and P. uncinata as sister species with basal P. uliginosa and asymmetric migration between all investigated species after their divergence. The magnitude of interspecies gene flow differed greatly, and it was consistently stronger from representatives of P. mugo complex to P. sylvestris than in the opposite direction. The results indicate the prominent role of reticulation evolution in those forest trees and provide a genetic framework to study species integrity maintained by selection and local adaptation.

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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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