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Abstract A species tree is a central concept in evolutionary biology whereby a single branching phylogeny reflects relationships among species. However, the phylogenies of different genomic regions often differ from the species tree. Although tree discordance is widespread in phylogenomic studies, we still lack a clear understanding of how variation in phylogenetic patterns is shaped by genome biology or the extent to which discordance may compromise comparative studies. We characterized patterns of phylogenomic discordance across the murine rodents—a large and ecologically diverse group that gave rise to the laboratory mouse and rat model systems. Combining recently published linked-read genome assemblies for seven murine species with other available rodent genomes, we first used ultraconserved elements (UCEs) to infer a robust time-calibrated species tree. We then used whole genomes to examine finer-scale patterns of discordance across ∼12 million years of divergence. We found that proximate chromosomal regions tended to have more similar phylogenetic histories. There was no clear relationship between local tree similarity and recombination rates in house mice, but we did observe a correlation between recombination rates and average similarity to the species tree. We also detected a strong influence of linked selection whereby purifying selection at UCEs led to appreciably less discordance. Finally, we show that assuming a single species tree can result in substantial deviation from the results with gene trees when testing for positive selection under different models. Collectively, our results highlight the complex relationship between phylogenetic inference and genome biology and underscore how failure to account for this complexity can mislead comparative genomic studies.
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Phylogenomic comparative methods: Accurate evolutionary inferences in the presence of gene tree discordance
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 genusSolanumwith 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.
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- Award ID(s):
- 1936187
- PAR ID:
- 10510506
- Publisher / Repository:
- National Academy of Sciences
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 120
- Issue:
- 22
- ISSN:
- 0027-8424
- Page Range / eLocation ID:
- e2220389120
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Thorne, Jeffrey (Ed.)Abstract Phylogenetic inference from genome-wide data (phylogenomics) has revolutionized the study of evolution because it enables accounting for discordance among evolutionary histories across the genome. To this end, summary methods have been developed to allow accurate and scalable inference of species trees from gene trees. However, most of these methods, including the widely used ASTRAL, can only handle single-copy gene trees and do not attempt to model gene duplication and gene loss. As a result, most phylogenomic studies have focused on single-copy genes and have discarded large parts of the data. Here, we first propose a measure of quartet similarity between single-copy and multicopy trees that accounts for orthology and paralogy. We then introduce a method called ASTRAL-Pro (ASTRAL for PaRalogs and Orthologs) to find the species tree that optimizes our quartet similarity measure using dynamic programing. By studying its performance on an extensive collection of simulated data sets and on real data sets, we show that ASTRAL-Pro is more accurate than alternative methods.more » « less
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null (Ed.)The 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 comparative methods do not account for discordance, resulting in incorrect inferences about the number, timing, and direction of trait transitions. 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 present a model that shows introgression makes hemiplasy more likely, such that methods that account for ILS alone will be conservative. We also present a method and software ( HeIST ) for making statistical inferences about the probability of hemiplasy and homoplasy in large datasets that contain both ILS and introgression. We apply our methods to two empirical datasets, finding that hemiplasy is likely to contribute to the observed trait incongruences in both.more » « less
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Abstract Phylogenomic analyses have increasingly adopted species tree reconstruction using methods that account for gene tree discordance using pipelines that require both human effort and computational resources. As the number of available genomes continues to increase, a new problem is facing researchers. Once more species become available, they have to repeat the whole process from the beginning because updating species trees is currently not possible. However, the de novo inference can be prohibitively costly in human effort or machine time. In this article, we introduce INSTRAL, a method that extends ASTRAL to enable phylogenetic placement. INSTRAL is designed to place a new species on an existing species tree after sequences from the new species have already been added to gene trees; thus, INSTRAL is complementary to existing placement methods that update gene trees. [ASTRAL; ILS; phylogenetic placement; species tree reconstruction.]more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.2220389120
