The role of hybridization and subsequent introgression has been demonstrated in an increasing number of species. Recently, Fontaine
This content will become publicly available on December 28, 2023
- Award ID(s):
- 1655683
- NSF-PAR ID:
- 10451914
- Editor(s):
- Ruane, Sara
- Date Published:
- Journal Name:
- Systematic Biology
- Volume:
- 72
- Issue:
- 1
- ISSN:
- 1063-5157
- Page Range / eLocation ID:
- 161 to 178
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract et al . (Science , 347, 2015, 1258524) conducted a phylogenomic analysis of six members of theAnopheles gambiae species complex. Their analysis revealed a reticulate evolutionary history and pointed to extensive introgression on all four autosomal arms. The study further highlighted the complex evolutionary signals that the co‐occurrence of incomplete lineage sorting (ILS ) and introgression can give rise to in phylogenomic analyses. While tree‐based methodologies were used in the study, phylogenetic networks provide a more natural model to capture reticulate evolutionary histories. In this work, we reanalyse theAnopheles data using a recently devised framework that combines the multispecies coalescent with phylogenetic networks. This framework allows us to captureILS and introgression simultaneously, and forms the basis for statistical methods for inferring reticulate evolutionary histories. The new analysis reveals a phylogenetic network with multiple hybridization events, some of which differ from those reported in the original study. To elucidate the extent and patterns of introgression across the genome, we devise a new method that quantifies the use of reticulation branches in the phylogenetic network by each genomic region. Applying the method to the mosquito data set reveals the evolutionary history of all the chromosomes. This study highlights the utility of ‘network thinking’ and the new insights it can uncover, in particular in phylogenomic analyses of large data sets with extensive gene tree incongruence. -
Kubatko, Laura (Ed.)Abstract Many recent phylogenetic methods have focused on accurately inferring species trees when there is gene tree discordance due to incomplete lineage sorting (ILS). For almost all of these methods, and for phylogenetic methods in general, the data for each locus are assumed to consist of orthologous, single-copy sequences. Loci that are present in more than a single copy in any of the studied genomes are excluded from the data. These steps greatly reduce the number of loci available for analysis. The question we seek to answer in this study is: what happens if one runs such species tree inference methods on data where paralogy is present, in addition to or without ILS being present? Through simulation studies and analyses of two large biological data sets, we show that running such methods on data with paralogs can still provide accurate results. We use multiple different methods, some of which are based directly on the multispecies coalescent model, and some of which have been proven to be statistically consistent under it. We also treat the paralogous loci in multiple ways: from explicitly denoting them as paralogs, to randomly selecting one copy per species. In all cases, the inferred species trees are as accurate as equivalent analyses using single-copy orthologs. Our results have significant implications for the use of ILS-aware phylogenomic analyses, demonstrating that they do not have to be restricted to single-copy loci. This will greatly increase the amount of data that can be used for phylogenetic inference.[Gene duplication and loss; incomplete lineage sorting; multispecies coalescent; orthology; paralogy.]more » « less
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Abstract Gene‐tree‐inference error can cause species‐tree‐inference artefacts in summary phylogenomic coalescent analyses. Here we integrate two ways of accommodating these inference errors: collapsing arbitrarily or dubiously resolved gene‐tree branches, and subsampling gene trees based on their pairwise congruence. We tested the effect of collapsing gene‐tree branches with 0% approximate‐likelihood‐ratio‐test (SH‐like aLRT) support in likelihood analyses and strict consensus trees for parsimony, and then subsampled those partially resolved trees based on congruence measures that do not penalize polytomies. For this purpose we developed a new TNT script for congruence sorting (
congsort ), and used it to calculate topological incongruence for eight phylogenomic datasets using three distance measures: standard Robinson–Foulds (RF) distances; overall success of resolution (OSR), which is based on counting both matching and contradicting clades; and RF contradictions, which only counts contradictory clades. As expected, we found that gene‐tree incongruence was often concentrated in clades that are arbitrarily or dubiously resolved and that there was greater congruence between the partially collapsed gene trees and the coalescent and concatenation topologies inferred from those genes. Coalescent branch lengths typically increased as the most incongruent gene trees were excluded, although branch supports typically did not. We investigated two successful and complementary approaches to prioritizing genes for investigation of alignment or homology errors. Coalescent‐tree clades that contradicted concatenation‐tree clades were generally less robust to gene‐tree subsampling than congruent clades. Our preferred approach to collapsing likelihood gene‐tree clades (0% SH‐like aLRT support) and subsampling those trees (OSR) generally outperformed competing approaches for a large fungal dataset with respect to branch lengths, support and congruence. We recommend widespread application of this approach (and strict consensus trees for parsimony‐based analyses) for improving quantification of gene‐tree congruence/conflict, estimating coalescent branch lengths, testing robustness of coalescent analyses to gene‐tree‐estimation error, and improving topological robustness of summary coalescent analyses. This approach is quick and easy to implement, even for huge datasets. -
Phylogenetic estimation under the multispecies coalescent model (MSCM) assumes all incongruence among loci is caused by incomplete lineage sorting. Therefore, applying the MSCM to datasets that contain incongruence that is caused by other processes, such as gene flow, can lead to biased phylogeny estimates. To identify possible bias when using the MSCM, we present P2C2M.SNAPP. P2C2M.SNAPP is an R package that identifies model violations using posterior predictive simulation. P2C2M.SNAPP uses the posterior distribution of species trees output by the software package SNAPP to simulate posterior predictive datasets under the MSCM, and then uses summary statistics to compare either the empirical data or the posterior distribution to the posterior predictive distribution to identify model violations. In simulation testing, P2C2M.SNAPP correctly classified up to 83% of datasets (depending on the summary statistic used) as to whether or not they violated the MSCM model. P2C2M.SNAPP represents a user-friendly way for researchers to perform posterior predictive model checks when using the popular SNAPP phylogenetic estimation program. It is freely available as an R package, along with additional program details and tutorials.more » « less
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Next-generation sequencing technologies have facilitated new phylogenomic approaches to help clarify previously intractable relationships while simultaneously highlighting the pervasive nature of incongruence within and among genomes that can complicate definitive taxonomic conclusions. Salvia L., with ∼1,000 species, makes up nearly 15% of the species diversity in the mint family and has attracted great interest from biologists across subdisciplines. Despite the great progress that has been achieved in discerning the placement of Salvia within Lamiaceae and in clarifying its infrageneric relationships through plastid, nuclear ribosomal, and nuclear single-copy genes, the incomplete resolution has left open major questions regarding the phylogenetic relationships among and within the subgenera, as well as to what extent the infrageneric relationships differ across genomes. We expanded a previously published anchored hybrid enrichment dataset of 35 exemplars of Salvia to 179 terminals. We also reconstructed nearly complete plastomes for these samples from off-target reads. We used these data to examine the concordance and discordance among the nuclear loci and between the nuclear and plastid genomes in detail, elucidating both broad-scale and species-level relationships within Salvia . We found that despite the widespread gene tree discordance, nuclear phylogenies reconstructed using concatenated, coalescent, and network-based approaches recover a common backbone topology. Moreover, all subgenera, except for Audibertia , are strongly supported as monophyletic in all analyses. The plastome genealogy is largely resolved and is congruent with the nuclear backbone. However, multiple analyses suggest that incomplete lineage sorting does not fully explain the gene tree discordance. Instead, horizontal gene flow has been important in both the deep and more recent history of Salvia . Our results provide a robust species tree of Salvia across phylogenetic scales and genomes. Future comparative analyses in the genus will need to account for the impacts of hybridization/introgression and incomplete lineage sorting in topology and divergence time estimation.more » « less
