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Contentious relationships in phylogenomic studies can be driven by a handful of genes
Open accessAbstract
Phylogenomic studies have resolved countless branches of the tree of life, but remain strongly contradictory on certain, contentious relationships. Here, we use a maximum likelihood framework to quantify the distribution of phylogenetic signal among genes and sites for 17 contentious branches and 6 well-established control branches in plant, animal and fungal phylogenomic data matrices. We find that resolution in some of these 17 branches rests on a single gene or a few sites, and that removal of a single gene in concatenation analyses or a single site from every gene in coalescence-based analyses diminishes support and can alter the inferred topology. These results suggest that tiny subsets of very large data matrices drive the resolution of specific internodes, providing a dissection of the distribution of support and observed incongruence in phylogenomic analyses. We submit that quantifying the distribution of phylogenetic signal in phylogenomic data is essential for evaluating whether branches, especially contentious ones, are truly resolved. Finally, we offer one detailed example of such an evaluation for the controversy regarding the earliest-branching metazoan phylum, for which examination of the distributions of gene-wise and site-wise phylogenetic signal across eight data matrices consistently supports ctenophores as the sister group to all other metazoans.
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“In order to assess the robustness of our age estimates to a number of prior assumptions, we ran analyses under (1) an autocorrelated and an uncorrelated relaxed molecular-clock model – the former assuming that the rate of molecular evolution of a lineage is correlated with the rate of its mother lineage, the latter allowing completely independent rates from lineage to lineage; (2) three different”
From Dating early animal evolution using phylogenomic data (2017) · cites this paper as [26]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“Use of other siteheterogeneous models that may not suffer from problems associated with CAT-F81 (see 24 and Supplementary Discussion) resulted in Ctenophora sister to all other animals 21 , consistent with our findings (Fig. 2, Supplementary Fig. S1-S14) and those of two recent papers that employed novel methods 25,26 .”
From Ctenophore relationships and their placement as the sister group to all other animals (2017) · cites this paper as [26]
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“This approach has, conversely, revealed underlying support favouring Ctenophora sister4,40, but so far has only been performed under standard site-homogeneous models.”
From Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding (2021) · cites this paper as [40]
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“Here, we have consolidated these findings by directly showing that the primary remaining lines of evidence supporting Ctenophora sister, partitioned phylogenomics4,7 and measures of underlying support (such as ΔPSlnl values)4,40, do not do so when better-fitting site-heterogeneous models are incorporated into the analysis.”
From Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding (2021) · cites this paper as [40]
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“This strategy has previously shown support for Ctenophora sister, in the form of a greater proportion of sites and gene partitions favouring comb jellies over sponges as the sister group to other animals4,40.”
From Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding (2021) · cites this paper as [40]
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“Quantifying and comparing support for alternative hypotheses for a given gene/site allows for dissection of the signal favouring one hypothesis or another in a dataset, and our results reject previous studies taking this approach that have found support for the Ctenophora-sister hypothesis4,40.”
From Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding (2021) · cites this paper as [40]
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“These irreversible FWM events provided powerful phylogenomic markers (97), offering strong evidence for resolving the long-debated relationships (104, 105) between ctenophores, sponges, and the rest of Metazoa.”
From Topological Approaches in Animal Comparative Genomics (2026) · cites this paper as [105]
In the citing paper
“Importantly, some of the differences between the results of RAxML/ExaML and IQ-TREE correspond to contentious relationships in phylogenomic studies (e.g., in data set ChenA4: The relative positions of pigeon, falcon, and other Neoaves; and in data set WickD3a: The relationships between Chloranthales, Eudicots, and Magnoliids) (Shen et al. 2017).”
From Evaluating fast maximum likelihood-based phylogenetic programs using empirical phylogenomic data sets (2018) · cites this paper as Shen et al. 2017
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“Shen et al. [11] generated datasets that excluded the few genes that they identified as ''outliers,''”
From Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals (2017) · cites this paper as [11]
In the citing paper
“analyzed these datasets under LG+G, and found support for Ctenophora-sister”
From Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals (2017) · cites this paper as [11]
In the citing paper
“This result rejects the conclusions of [11] that signal for Porifera-sister is limited to ''outlier genes'' and indicates that their approach is model dependent: arguments about model adequacy should be considered when implementing it.”
From Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals (2017) · cites this paper as [11]
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“LG+G was used by [11]”
From Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals (2017) · cites this paper as [11]
In the citing paper
“Indeed, CAT-GTR+G analyses (with and without Dayhoff-6 recoding) of a dataset of [10] from which [11] removed ''outlier genes'' still finds support for Porifera-sister (PP = 0.98 and PP = 0.99, respectively; Figures S3I and S3J).”
From Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals (2017) · cites this paper as [11]
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Metadata
- Authors
- Shen, X.-X., Hittinger, C. T., & Rokas, A.
- Affiliations
- Vanderbilt University (US)
- University of Wisconsin–Madison (US)
- Corresponding author
- Rokas, Antonis
- Venue
- Nature Ecology & Evolution
- Published
- 2017-04-10
- Volume
- 1
- Issue
- 5
- Pages
- 126-126
- ISSN
- 2397-334X (ISSN-L)
- PMC
- PMC5560076
- OpenAlex
- W2607411230
- Semantic Scholar
- 1a74377821782786bf6787cb988e289469f977ac
- Cited by
- 520
- References
- 62
- Citations by year
- 2026: 25 · 2025: 39 · 2024: 41 · 2023: 49 · 2022: 36 · 2021: 67 · 2020: 70 · 2019: 78 · 2018: 74 · 2017: 41
- FWCI
- 29.45
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature Ecology & Evolution (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- Funders
- National Science Foundation (1442148, BER DE-FC02-07ER64494, 1003258, 1442113)
- U.S. Department of Energy (FC02-07ER64494, 07ER64494, DEFC0207ER64494, BER DE‐FC02‐07ER64494)
- U.S. Department of Agriculture (DE-FC02-07ER64494)
- Vanderbilt University
- National Institutes of Health
- National Institute of Food and Agriculture (1003258, DE-FC02-07ER64494)
- Office of Science (BER DE-FC02-07ER64494, FC02-07ER64494, DEFC0207ER64494)
- Great Lakes Bioenergy Research Center (BER-DE-FC02-07ER64494, DE‐FC02‐07ER64494)
- National Institute of Allergy and Infectious Diseases (AI105619, R21AI105619)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Keywords
- phylogenetic incongruence, ctenophores, phylogenomics, phylogenetic support
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