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

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

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.]

2019 ◽  
Vol 69 (3) ◽  
pp. 593-601 ◽  
Author(s):  
Christopher Blair ◽  
Cécile Ané

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.


2020 ◽  
Author(s):  
Liming Cai ◽  
Zhenxiang Xi ◽  
Emily Moriarty Lemmon ◽  
Alan R Lemmon ◽  
Austin Mast ◽  
...  

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.


2021 ◽  
Author(s):  
Caitlin Cherryh ◽  
Bui Quang Minh ◽  
Rob Lanfear

AbstractMost phylogenetic analyses assume that the evolutionary history of an alignment (either that of a single locus, or of multiple concatenated loci) can be described by a single bifurcating tree, the so-called the treelikeness assumption. Treelikeness can be violated by biological events such as recombination, introgression, or incomplete lineage sorting, and by systematic errors in phylogenetic analyses. The incorrect assumption of treelikeness may then mislead phylogenetic inferences. To quantify and test for treelikeness in alignments, we develop a test statistic which we call the tree proportion. This statistic quantifies the proportion of the edge weights in a phylogenetic network that are represented in a bifurcating phylogenetic tree of the same alignment. We extend this statistic to a statistical test of treelikeness using a parametric bootstrap. We use extensive simulations to compare tree proportion to a range of related approaches. We show that tree proportion successfully identifies non-treelikeness in a wide range of simulation scenarios, and discuss its strengths and weaknesses compared to other approaches. The power of the tree-proportion test to reject non-treelike alignments can be lower than some other approaches, but these approaches tend to be limited in their scope and/or the ease with which they can be interpreted. Our recommendation is to test treelikeness of sequence alignments with both tree proportion and mosaic methods such as 3Seq. The scripts necessary to replicate this study are available at https://github.com/caitlinch/treelikeness


Author(s):  
Leonardo S Miranda ◽  
Bernardo O Prestes ◽  
Alexandre Aleixo

Abstract Here we use an integrative approach, including coalescent-based methods, isolation–migration and species distribution models, to infer population structure, divergence times and diversification in the two species of the genus Cymbilaimus (Aves, Thamnophilidae). Our results support a recent and rapid diversification with both incomplete lineage sorting and gene flow shaping the evolutionary history of Cymbilaimus. The spatio-temporal pattern of cladogenesis suggests that Cymbilaimus originated in the north/western portion of cis-Andean South America and then diversified into the Brazilian Shield and Central America after consolidation of the modern Amazonian drainage and the Andean range. This evolutionary scenario is explained by cycles of range expansion and dispersal, followed by isolation, and recurrent gene flow, during the last 1.2 Myr. Our results agree with those recently reported for other closely related suboscine lineages, whereby the window of introgression between closely related taxa remains open for up to a few million years after their original split. In Cymbilaimus, introgression was recurrent between C. lineatus and C. sanctaemariae, even after they acquired vocal and ecological differentiation, supporting the claim that at least in Neotropical suboscines, full reproductive compatibility may take millions of years to evolve and cannot be interpreted as synonymous with a lack of speciation.


Diversity ◽  
2018 ◽  
Vol 10 (3) ◽  
pp. 65 ◽  
Author(s):  
Thierry Grange ◽  
Jean-Philip Brugal ◽  
Laurence Flori ◽  
Mathieu Gautier ◽  
Antigone Uzunidis ◽  
...  

Knowledge about the origin and evolutionary history of the bison has been improved recently owing to several genomic and paleogenomic studies published in the last two years, which elucidated large parts of the evolution of bison populations during the Upper Pleistocene and Holocene in Eurasia. The produced data, however, were interpreted in contradicting manners. Here, we have gathered, reanalyzed and compared previously published or unpublished morphometric and genetic data that have not yet been integrated and that we synthesize in a unified framework. In particular, we re-estimate dates of divergence of mitogenome lineages based on an extended dataset comprising 81 complete ancient bison mitogenomes and we revisit putative gene flow between the Bos and Bison genera based on comparative analyses of ancient and modern bison genomes, thereby questioning published conclusions. Morphometric analyses taking into account sexual dimorphism invalidate a previous claim that Bison schoetensacki was present in France during the Late Pleistocene. Both morphometric and genome analyses reveal that Eurasian bison belonging to different Bison priscus and Bison bonasus lineages maintained parallel evolutionary paths with gene flow during a long period of incomplete speciation that ceased only upon the migration of B. priscus to the American continent establishing the American bison lineage. Our nuclear genome analysis of the evolutionary history of B. bonasus allows us to reject the previous hypothesis that it is a hybrid of B. priscus and Bos primigenius. Based on present-day behavioral studies of European and American bison, we propose that apparently conflicting lines of evidence can be reconciled by positing that female bison drove the specialization of bison populations to different ecological niches while male bison drove regular homogenizing genetic exchanges between populations.


Genome ◽  
2014 ◽  
Vol 57 (2) ◽  
pp. 97-109 ◽  
Author(s):  
Chi Yan ◽  
Qianni Hu ◽  
Genlou Sun

Evidence accumulated over the last decade has shown that allopolyploid genomes may undergo complex reticulate evolution. In this study, 13 accessions of tetraploid Elymus pendulinus were analyzed using two low-copy nuclear genes (RPB2 and PepC) and two regions of chloroplast genome (Rps16 and trnD-trnT). Previous studies suggested that Pseudoroegneria (St) and an unknown diploid (Y) were genome donors to E. pendulinus, and that Pseudoroegneria was the maternal donor. Our results revealed an extreme reticulate pattern, with at least four distinct gene lineages coexisting within this species that might be acquired through a possible combination of allotetraploidization and introgression from both within and outside the tribe Hordeeae. Chloroplast DNA data identified two potential maternal genome donors (Pseudoroegneria and an unknown species outside Hordeeae) to E. pendulinus. Nuclear gene data indicated that both Pseudoroegneria and an unknown Y diploid have contributed to the nuclear genome of E. pendulinus, in agreement with cytogenetic data. However, unexpected contributions from Hordeum and unknown aliens from within or outside Hordeeae to E. pendulinus without genome duplication were observed. Elymus pendulinus provides a remarkable instance of the previously unsuspected chimerical nature of some plant genomes and the resulting phylogenetic complexity produced by multiple historical reticulation events.


Author(s):  
Maddie E. James ◽  
Henry Arenas-Castro ◽  
Jeffery S. Groh ◽  
Jan Engelstädter ◽  
Daniel Ortiz-Barrientos

AbstractParallel evolution of ecotypes occurs when selection independently drives the evolution of similar traits across similar environments. The multiple origin of ecotypes is often inferred on the basis of a phylogeny which clusters populations according to geographic location and not by the environment they occupy. However, the use of phylogenies to infer parallel evolution in closely related populations is problematic due to the potential for gene flow and incomplete lineage sorting to uncouple the genetic structure at neutral markers from the colonization history of populations. Here, we demonstrate multiple origins within ecotypes of an Australian wildflower, Senecio lautus. We observed strong genetic structure as well as phylogenetic clustering by geography, and show this is unlikely due to gene flow between parapatric ecotypes, which is surprisingly low. We further confirm this analytically by demonstrating that phylogenetic distortion due to gene flow often requires higher levels of migration than those observed in S. lautus. Our results imply that selection can repeatedly create similar phenotypes despite the perceived homogenizing effects of gene flow.


2018 ◽  
Author(s):  
Kunal Arekar ◽  
Abhijna Parigi ◽  
K. Praveen Karanth

AbstractEvolutionary studies have traditionally relied on concatenation based methods to reconstruct relationships from multiple markers. However, due to limitations of concatenation analyses, recent studies have proposed coalescent based methods to address evolutionary questions. Results from these methods tend to diverge from each other under situations where there is incomplete lineage sorting or hybridization. Here we used concatenation as well as multispecies coalescent (MSC) methods to understand the evolutionary origin of capped and golden langur (CG) lineage. Previous molecular studies have retrieved conflicting phylogenies, with mitochondrial tree grouping CG lineage with a largely Indian genus Semnopithecus, while nuclear markers support their affinities with a Southeast Asian genus, Trachypithecus. However, as pointed by others, the use of nuclear copies of mitochondrial DNA in the above studies might have generated the discordance. Because of this discordance, the phylogenetic position of CG lineage has been much debated in recent times. In this study, we have used nine nuclear and eight mitochondrial markers. Concatenated nuclear as well as the mitochondrial dataset recovered congruent relationships where CG lineage was sister to Trachypithecus. However nuclear species tree estimated using different MSC methods were incongruent with the above result, suggesting presence of incomplete lineage sorting (ILS)/hybridisation. Furthermore, CG lineage is morphologically intermediate between Semnopithecus and Trachypithecus. Based on this evidence, we argue that CG lineage evolved through hybridisation between Semnopithecus and Trachypithecus. Finally, we reason that both concatenation as well as coalescent methods should be used in conjunction for better understanding of various evolutionary hypotheses.


Author(s):  
Amanda Patsis ◽  
Rick P. Overson ◽  
Krissa A. Skogen ◽  
Norman J. Wickett ◽  
Matthew G. Johnson ◽  
...  

Oenothera sect. Pachylophus has proven to be a valuable system in which to study plant-insect coevolution and the drivers of variation in floral morphology and scent. Current species circumscriptions based on morphological characteristics suggest that the section consists of five species, one of which is subdivided into five subspecies. Previous attempts to understand species (and subspecies) relationships at amolecular level have been largely unsuccessful due to high levels of incomplete lineage sorting and limited phylogenetic signal from slowly evolving gene regions. In the present study, target enrichment was used to sequence 322 conserved protein-coding nuclear genes from 50 individuals spanning the geographic range of Oenothera sect. Pachylophus, with species trees inferred using concatenation and coalescentbasedmethods. Our findings concur with previous research in suggesting that O. psammophila and O. harringtonii are nested within a paraphyleticOenothera cespitosa. By contrast, our results show clearly that the two annual species (O. cavernae and O. brandegeei) did not arise from the O. cespitosa lineage, but rather from a common ancestor of Oenothera sect. Pachylophus. Budding speciation as a result of edaphic specializationappears to best explain the evolution of the narrow endemic species O. harringtonii and O. psammophila. Complete understanding of possible introgression among subspecies of O. cespitosa will require broader sampling across the full geographical and ecological ranges of these taxa.


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