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Phylogenetic comparative methods have long been a mainstay of evolutionary biology, allowing for the study of trait evolution across species while accounting for their common ancestry. These analyses typically assume a single, bifurcating phylogenetic tree describing the shared history among species. However, modern phylogenomic analyses have shown that genomes are often composed of mosaic histories that can disagree both with the species tree and with each other—so-called discordant gene trees. These gene trees describe shared histories that are not captured by the species tree, and therefore that are unaccounted for in classic comparative approaches. The application of standard comparative methods to species histories containing discordance leads to incorrect inferences about the timing, direction, and rate of evolution. Here, we develop two approaches for incorporating gene tree histories into comparative methods: one that constructs an updated phylogenetic variance–covariance matrix from gene trees, and another that applies Felsenstein's pruning algorithm over a set of gene trees to calculate trait histories and likelihoods. Using simulation, we demonstrate that our approaches generate much more accurate estimates of tree- wide rates of trait evolution than standard methods. We apply our methods to two clades of the wild tomato genus Solanum with varying rates of discordance, demonstrating the contribution of gene tree discordance to variation in a set of floral traits. Our approaches have the potential to be applied to a broad range of classic inference problems in phylogenetics, including ancestral state reconstruction and the inference of lineage- specific rate shifts.

Incongruence, or topological conflict, is prevalent in genome-scale data sets. Internode certainty (IC) and related measures were recently introduced to explicitly quantify the level of incongruence of a given internal branch among a set of phylogenetic trees and complement regular branch support measures (e.g., bootstrap, posterior probability) that instead assess the statistical confidence of inference. Since most phylogenomic studies contain data partitions (e.g., genes) with missing taxa and IC scores stem from the frequencies of bipartitions (or splits) on a set of trees, IC score calculation typically requires adjusting the frequencies of bipartitions from these partial gene trees. However, when the proportion of missing taxa is high, the scores yielded by current approaches that adjust bipartition frequencies in partial gene trees differ substantially from each other and tend to be overestimates. To overcome these issues, we developed three new IC measures based on the frequencies of quartets, which naturally apply to both complete and partial trees. Comparison of our new quartet-based measures to previous bipartition-based measures on simulated data shows that: (1) on complete data sets, both quartet-based and bipartition-based measures yield very similar IC scores; (2) IC scores of quartet-based measures on a given data set with and without missing taxa are more similar than the scores of bipartition-based measures; and (3) quartet-based measures are more robust to the absence of phylogenetic signal and errors in phylogenetic inference than bipartition-based measures. Additionally, the analysis of an empirical mammalian phylogenomic data set using our quartet-based measures reveals the presence of substantial levels of incongruence for numerous internal branches. An efficient open-source implementation of these quartet-based measures is freely available in the program QuartetScores (https://github.com/lutteropp/QuartetScores).

Abstract An important goal of evolutionary genomics is to identify genomic regions whose substitution rates differ among lineages. For example, genomic regions experiencing accelerated molecular evolution in some lineages may provide insight into links between genotype and phenotype. Several comparative genomics methods have been developed to identify genomic accelerations between species, including a Bayesian method called PhyloAcc, which models shifts in substitution rate in multiple target lineages on a phylogeny. However, few methods consider the possibility of discordance between the trees of individual loci and the species tree due to incomplete lineage sorting, which might cause false positives. Here, we present PhyloAcc-GT, which extends PhyloAcc by modeling gene tree heterogeneity. Given a species tree, we adopt the multispecies coalescent model as the prior distribution of gene trees, use Markov chain Monte Carlo (MCMC) for inference, and design novel MCMC moves to sample gene trees efficiently. Through extensive simulations, we show that PhyloAcc-GT outperforms PhyloAcc and other methods in identifying target lineage-specific accelerations and detecting complex patterns of rate shifts, and is robust to specification of population size parameters. PhyloAcc-GT is usually more conservative than PhyloAcc in calling convergent rate shifts because it identifies more accelerations on ancestral than on terminal branches. We apply PhyloAcc-GT to two examples of convergent evolution: flightlessness in ratites and marine mammal adaptations, and show that PhyloAcc-GT is a robust tool to identify shifts in substitution rate associated with specific target lineages while accounting for incomplete lineage sorting.

Abstract Even in the genomics era, the phylogeny of Neotropical small felids comprised in the genus Leopardus remains contentious. We used whole-genome resequencing data to construct a time-calibrated consensus phylogeny of this group, quantify phylogenomic discordance, test for interspecies introgression, and assess patterns of genetic diversity and demographic history. We infer that the Leopardus radiation started in the Early Pliocene as an initial speciation burst, followed by another in its subgenus Oncifelis during the Early Pleistocene. Our findings challenge the long-held notion that ocelot (Leopardus pardalis) and margay (L. wiedii) are sister species and instead indicate that margay is most closely related to the enigmatic Andean cat (L. jacobita), whose whole-genome data are reported here for the first time. In addition, we found that the newly sampled Andean tiger cat (L. tigrinus pardinoides) population from Colombia associates closely with Central American tiger cats (L. tigrinus oncilla). Genealogical discordance was largely attributable to incomplete lineage sorting, yet was augmented by strong gene flow between ocelot and the ancestral branch of Oncifelis, as well as between Geoffroy's cat (L. geoffroyi) and southern tiger cat (L. guttulus). Contrasting demographic trajectories have led to disparate levels of current genomic diversity, with a nearly tenfold difference in heterozygosity between Andean cat and ocelot, spanning the entire range of variability found in extant felids. Our analyses improved our understanding of the speciation history and diversity patterns in this felid radiation, and highlight the benefits to phylogenomic inference of embracing the many heterogeneous signals scattered across the genome.

Background Plastome-scale data have been prevalent in reconstructing the plant Tree of Life. However, phylogenomic studies currently based on plastomes rely primarily on maximum likelihood inference of concatenated alignments of plastid genes, and thus phylogenetic discordance produced by individual plastid genes has generally been ignored. Moreover, structural and functional characteristics of plastomes indicate that plastid genes may not evolve as a single locus and are experiencing different evolutionary forces, yet the genetic characteristics of plastid genes within a lineage remain poorly studied. Results We sequenced and annotated 10 plastome sequences of Gentianeae. Phylogenomic analyses yielded robust relationships among genera within Gentianeae. We detected great variation of gene tree topologies and revealed that more than half of the genes, including one ( atpB ) of the three widely used plastid markers ( rbcL , atpB and matK ) in phylogenetic inference of Gentianeae, are likely contributing to phylogenetic ambiguity of Gentianeae. Estimation of nucleotide substitution rates showed extensive rate heterogeneity among different plastid genes and among different functional groups of genes. Comparative analysis suggested that the ribosomal protein (RPL and RPS) genes and the RNA polymerase (RPO) genes have higher substitution rates and genetic variations among plastid genes in Gentianeae. Our study revealed that just one ( matK ) of the three ( matK, ndhB and rbcL ) widely used markers show high phylogenetic informativeness (PI) value. Due to the high PI and lowest gene-tree discordance, rpoC2 is advocated as a promising plastid DNA barcode for taxonomic studies of Gentianeae. Furthermore, our analyses revealed a positive correlation of evolutionary rates with genetic variation of plastid genes, but a negative correlation with gene-tree discordance under purifying selection. Conclusions Overall, our results demonstrate the heterogeneity of nucleotide substitution rates and genetic characteristics among plastid genes providing new insights into plastome evolution, while highlighting the necessity of considering gene-tree discordance into phylogenomic studies based on plastome-scale data.

AimA number of processes can lead to weak or conflicting phylogenetic signals, especially in geographically dynamic regions where unstable landscapes and climates promote complex evolutionary histories. The Middle American pitviper genus Bothriechis has a complex biogeographic distribution and previous phylogenetic analyses have recovered conflicting topologies based on the data type used. Here, we tested whether historic conflicts in the phylogeny were the result of reticulate evolution and whether the inferred biogeographic history of the group would enable contact among reticulate lineages.LocationMiddle America.TaxonPalm‐pitvipers (genus Bothriechis).MethodsWe generated a phylogenomic dataset using an anchored phylogenomics approach and inferred a genomics‐based species tree and mitochondrial tree to assess incongruence among datasets. We then generated a dated phylogeny and conducted ancestral area reconstruction to examine the biogeographic history surrounding the diversification of these species. We additionally tested whether the discordance among trees is better explained by lineage sorting or reticulate evolution by testing models of reticulate evolution inferred through multiple methods.ResultsWe found strong support for discordance in the phylogeny of Bothriechis and corresponding evidence for reticulate evolution among lineages with incongruent placement. Ancestral area reconstruction placed these taxa in adjacent regions during the time period when reticulation was projected to take place and suggested a biogeographic history heavily influenced by vicariant processes.Main conclusionsReticulation among geographically proximate lineages has driven apparent genomic discordance in Bothriechis and is responsible for historical incongruence in the phylogeny. Inference of the order of events suggests that reticulation among nuclear Middle American taxa occurred during a time of geologic upheaval, promoting lineage divergence and secondary contact. Reticulate evolution and similar processes can have substantial impacts on the evolutionary trajectory of taxa and are important to explicitly test for in biogeographically complex regions.

Phylogenomic data enriched with informative loci have significantly improved phylogenetic resolution and facilitated the elucidation of evolutionary mechanisms underlying phylogenetic discordance. Species of the East Asian lineage (EAL) within the Allium subgenus Anguinum are widespread in the Himalaya–Hengduan Mountains (HHMs), which exhibit long-standing taxonomic ambiguity and phylogenetic discordance, calling for investigation. In this study, we collected 102 samples, including 45 transcriptomes and 57 plastid genomes, covering multiple populations of all currently recognized taxa within the EAL and relatives. A total of 2,186 low-copy nuclear genes (LCGs) and 163 plastid sequences (including 111 genes and 52 intergenic regions) were employed for phylogenetic analyses. Our results revealed that the EAL is a monophyletic taxon but exhibits a polytomous phylogeny, it further divides into four sublineages in the LCG-based tree and two sublineages in the plastid-based tree, which display distinct geographical distribution patterns. Samples of A. ovalifolium var. leuconeurum , A. ovalifolium var. cordifolium and A. funckiifolium from the northwest Sichuan Basin and Qinling-Daba Mountains clustered within the A. ovalifolium samples of these regions, while A. nanodes is entirely embedded within the HHMs populations of A. prattii and A. ovalifolium . Extensive phylogenetic conflicts were detected within EAL, and the ancestral area reconstruction indicates that the EAL originated in the Hengduan Mountains (HDMs). Morphological and phylogenetic evidence confirmed the varietal status of A. ovalifolium var. leuconeurum and A. ovalifolium var. cordifolium , while also proposing the reclassification of A. funckiifolium as A. ovalifolium var. funckiifolium . The observed polytomous phylogeny within EAL is likely attributed to rapid radiations triggered by geological events and climatic fluctuations during the late Pliocene and Pleistocene, coupled with recurrent isolation–contact dynamics, which resulted in the retention of ancestral polymorphisms and historical gene flow. Widespread phylogenetic discordance in the EAL is mainly due to incomplete lineage sorting (ILS), with hybridization also playing key roles. This study not only reveals the underlying causes of taxonomic controversies within the EAL but also provides critical insights into the unique phylogenetic patterns and evolutionary mechanisms shaping plant lineages in the HHMs biodiversity hotspot.

The evolutionary history of Ephedra L. has over time proved to be a very difficult phylogenetic problem, something which probably is best reflected by the incongruent phylogenetic relationships demonstrated in and among previous studies. A low number of phylogenetically informative sites and different rooting strategies have been suggested as explanations, but the role of gene tree discordance and its underlying causes and influence on phylogenetic reconstruction in Ephedra have largely remained unexplored. In the present study, we address the phylogeny of Ephedra using information from a large set of nuclear low‐copy genes obtained with a specifically designed bait set. We explore the potential effect of putative paralogy, intra‐locus recombination, and chimeric sequences on phylogenetic estimation in Ephedra, while striving to minimize the risk for gene tree error. Our results indicate that recombination and putatively paralogous sequences have limited influence on phylogenetic results, although handling of putative paralogs and recombinants did improve overall species tree resolution and statistics. A robust Ephedra species phylogeny was obtained by analyzing gene trees, in which orthologous clades were inferred from data composed of orthologous and putatively paralogous sequences. The results support the division of Ephedra into three geographically defined clades, with the American clade as sister to the Mediterranean clade and the Asian clade. Relationships among species within these three clades were relatively consistent among our analytical approaches, but our results highlighted moderate to strong signals of gene tree discordance at many branches including the deepest split. Incomplete lineage sorting is a possible explanation for this discord for many branches, but hybridization/introgression is also commonly indicated. Low‐copy nuclear genes were used to address the notoriously difficult phylogeny of Ephedra. Additionally, we explored the potential effect of putative paralogy, intra‐locus recombination, and chimeric sequences on phylogenetic estimation.