Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals

In the paper

“In contrast, WhelanD20-Holo, the dataset from which fungal outgroups were excluded, and WhelanD20-Choano, the dataset from which all outgroups but the Choanoflagellata were excluded, supported Porifera-sister (PP = 0.68 and PP = 0.77, respectively; Table 3; Figures S2B and S3B).”

In the paper

“However, all models, including CAT-GTR+G, were strongly rejected-with the smallest absolute Z score ( j Z j = 12.15) obtained from the CAT-GTR+G analysis of Chang.”

In the paper

“With both tests, CAT-GTR+G obtained the lowest Z scores, and PF-schemes emerged as the second best modeling strategy”

In the paper

“Our results show that support for Ctenophora-sister decreases, while at the same time support for Porifera-sister increases, when heterogeneity in the data is better accounted for.”

In the paper

“All recoded datasets obtained lower Z scores than the original amino acid datasets for both PPA-MAX and PPAMEAN (Tables 1 and S1), indicating that recoding is effective at reducing lineage-specific compositional heterogeneity.”

In the paper

“For KGB-6, the PP for Porifera-sister was 0.78 for Chang and 0.68 for WhelanD20-Holo.”

In the paper

“Under CAT-GTR+G, only PPA-DIV invariably recovered reduced Z scores from the recoded datasets (Table 1), with Z scores from PPA-CONV and PPA-VAR being similar in analyses performed with and without recoding (Table S1).”

In the paper

“Similarly, phylogenies inferred from Chang using PF-scheme and CAT-GTR+G (see STAR Methods) supported Ctenophora-sister with 100% bootstrap support and PP z 1, respectively”

In the paper

“Support for Ctenophora-sister was severely reduced in CATGTR+Ganalyses of both recoded datasets, with support for Porifera-sister being higher than that for Ctenophora-sister”

In the paper

“More broadly, our results demonstrate that PFschemes (strongly advocated for by [10, 28, 29, 38]) are much worse than CAT-GTR+G and are not always better than unpartitioned modeling strategies at capturing the heterogeneity of the considered datasets”

What the sources say

• Not checked yetcites [10] Whelan, 2015, Error, signal, and the placement of Ctenophora sister to all other animals, Proc. Natl. Acad. Sci. USA source
• Not checked yetcites [28] Halanych, 2016, Miscues misplace sponges, Proc. Natl. Acad. Sci. USA source
• Not checked yetcites [29] Whelan, 2017, Who let the CAT out of the bag? Accurately dealing with substitutional heterogeneity in phylogenomic analyses, Syst. Biol.
• Not checked yetcites [38] Whelan, 2017, Ctenophore relationships and their placement as the sister group to all other animals, Nat. Ecol. Evol. source

In the paper

“WAG+G, LG+G, GTR+G (with or without recoding), and PF-schemes describe the data worse than CAT-GTR+G and invariably found support for Ctenophora-sister.”

In the paper

“Indeed, a CAT-GTR+G analysis of the Dayhoff-6 recoded version of this dataset reached excellent convergence and found strong support for Porifera-sister (PP = 1; Figure S3K)”

What the sources say

• Not checked yetcites [38] Whelan, 2017, Ctenophore relationships and their placement as the sister group to all other animals, Nat. Ecol. Evol. source

In the paper

“Data recoding reduced the impact of heterogeneity on our phylogenetic analyses (see also [7]), and this lent support to Porifera-sister. Notably, this result emerged independently of the outgroups included.”

What the sources say

• Not checked yetcites [7] Simion, 2017, A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals, Curr. Biol. source

In the paper

“Phylogenetic analyses of early animal relationships using models that do not describe site-specific amino acid differences (WAG+G, LG+G, GTR+G, and optimal PF-schemes) invariably support Ctenophora-sister, whereas analyses using models that can accommodate such preferences (e.g., CAT-GTR+G) predominantely favor Porifera-sister.”

In the paper

“Our PPA tests indicate that although CAT-GTR+G describes Chang and WhelanD20 better than other models, overall model adequacy can still be improved using data recoding, and Porifera-sister was favored under all recoding strategies.”

In the paper

“However, phylogenomic analyses have supported both Porifera-sister [6, 7, 39, 41-44] and Ctenophora-sister [8-12, 35, 45, 46], with some studies (like [47]) presenting both trees.”

What the sources say

• Not checked yetcites [6] Pisani, 2015, Genomic data do not support comb jellies as the sister group to all other animals, Proc. Natl. Acad. Sci. USA source
• Not checked yetcites [7] Simion, 2017, A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals, Curr. Biol. source
• Not checked yetcites [39] Nosenko, 2013, Deep metazoan phylogeny: when different genes tell different stories, Mol. Phylogenet. Evol. source
• Not checked yetcites [41] Philippe, 2009, Phylogenomics revives traditional views on deep animal relationships, Curr. Biol. source
• Not checked yetcites [42] Pick, 2010, Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships, Mol. Biol. Evol. source
• Not checked yetcites [43] Philippe, 2011, Resolving difficult phylogenetic questions: why more sequences are not enough, PLoS Biol. source
• Not checked yetcites [44] Eitel, 2017, A taxogenomics approach uncovers a new genus in the phylum Placozoa, bioRxiv
• Not checked yetcites [8] Ryan, 2013, The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution, Science source
• Not checked yetcites [9] Moroz, 2014, The ctenophore genome and the evolutionary origins of neural systems, Nature source
• Not checked yetcites [10] Whelan, 2015, Error, signal, and the placement of Ctenophora sister to all other animals, Proc. Natl. Acad. Sci. USA source

In the paper

“Across-site replacement-pattern heterogeneity [26] and compositional heterogeneity across taxa [13, 55] can both have a misleading effect on phylogenetic reconstruction.”

What the sources say

• Not checked yetcites [26] Lartillot, 2007, Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model, BMC Evol. Biol. source
• Not checked yetcites [13] Hrdy, 2004, Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I, Nature source
• Not checked yetcites [55] Foster, 2004, Modeling compositional heterogeneity, Syst. Biol. source

In the paper

“Ctenophora-sister invariably emerges when site-specific amino acid differences are not modeled [10] or when site-specific amino acid differences are modeled but distant outgroups are used to root the tree [6].”

What the sources say

• Not checked yetcites [10] Whelan, 2015, Error, signal, and the placement of Ctenophora sister to all other animals, Proc. Natl. Acad. Sci. USA source
• Not checked yetcites [6] Pisani, 2015, Genomic data do not support comb jellies as the sister group to all other animals, Proc. Natl. Acad. Sci. USA source

In the paper

“To minimize systematic error, it is important to use the evolutionary model that best fits the data [18, 48-50].”

What the sources say

• Not checked yetcites [18] Heath, 2008, Taxon sampling and the accuracy of phylogenetic analyses, J. Syst. Evol.
• Not checked yetcites [48] Posada, 1998, MODELTEST: testing the model of DNA substitution, Bioinformatics source
• Not checked yetcites [49] Cunningham, 1998, Best-fit maximum-likelihood models for phylogenetic inference: empirical tests with known phylogenies, Evolution
• Not checked yetcites [50] Sullivan, 2005, Model selection in phylogenetics, Annu. Rev. Ecol. Evol. Syst. source

In the paper

“Shen et al. [11] generated datasets that excluded the few genes that they identified as ''outliers,''”

What the sources say

• Not checked yetcites [11] Shen, 2017, Contentious relationships in phylogenomic studies can be driven by a handful of genes, Nat Ecol Evol source

In the 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.”

What the sources say

• Not checked yetcites [11] Shen, 2017, Contentious relationships in phylogenomic studies can be driven by a handful of genes, Nat Ecol Evol source

In the paper

“WhelanD20 was not analyzed under its optimal PF-scheme because [10] already showed that this dataset supports Ctenophora-sister when the PF-scheme is used.”

What the sources say

• Not checked yetcites [10] Whelan, 2015, Error, signal, and the placement of Ctenophora sister to all other animals, Proc. Natl. Acad. Sci. USA source

In the paper

“GTR+G was used by [8]”

What the sources say

• Not checked yetcites [8] Ryan, 2013, The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution, Science source

In the paper

“analyzed these datasets under LG+G, and found support for Ctenophora-sister”

What the sources say

• Not checked yetcites [11] Shen, 2017, Contentious relationships in phylogenomic studies can be driven by a handful of genes, Nat Ecol Evol source

In the paper

“The second is a dataset from [10] that had not been reassessed in [6].”

What the sources say

• Not checked yetcites [10] Whelan, 2015, Error, signal, and the placement of Ctenophora sister to all other animals, Proc. Natl. Acad. Sci. USA source
• Not checked yetcites [6] Pisani, 2015, Genomic data do not support comb jellies as the sister group to all other animals, Proc. Natl. Acad. Sci. USA source

In the paper

“WAG+G was used by [9]”

What the sources say

• Not checked yetcites [9] Moroz, 2014, The ctenophore genome and the evolutionary origins of neural systems, Nature source

In the paper

“Branch length is the product of time and substitution rate, and even slowly evolving outgroups can be long branched if they diverged much earlier than the ingroup, potentially exacerbating long-branch attraction artifacts [18, 57].”

What the sources say

• Not checked yetcites [18] Heath, 2008, Taxon sampling and the accuracy of phylogenetic analyses, J. Syst. Evol.
• Not checked yetcites [57] Hillis, 1998, Taxonomic sampling, phylogenetic accuracy, and investigator bias, Syst. Biol. source

In the paper

“LG+G was used by [11]”

What the sources say

• Not checked yetcites [11] Shen, 2017, Contentious relationships in phylogenomic studies can be driven by a handful of genes, Nat Ecol Evol source

In the paper

“Whelan et al. [38] have increased the number of ctenophoran species compared to those they used in [10].”

What the sources say

• Not checked yetcites [38] Whelan, 2017, Ctenophore relationships and their placement as the sister group to all other animals, Nat. Ecol. Evol. source
• Not checked yetcites [10] Whelan, 2015, Error, signal, and the placement of Ctenophora sister to all other animals, Proc. Natl. Acad. Sci. USA source

In the paper

“Chang was analyzed under its optimal PF-scheme using RAxML version 8.2.9 [63], with support estimated using the rapid bootstrap option (100 replicates).”

What the sources say

• Not checked yetcites [63] Stamatakis, 2014, RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies, Bioinformatics source

In the paper

“The number of samples to be discarded as burnin was independently assessed for each analysis by visually checking traces of likelihood and parameter values.”

In the paper

“which is very similar to WhelanD20”

What the sources say

• Not checked yetcites [10] Whelan, 2015, Error, signal, and the placement of Ctenophora sister to all other animals, Proc. Natl. Acad. Sci. USA source

In the paper

“which apparently explicitly excludes proteins of significant compositional heterogeneity (see [10])”

What the sources say

• Not checked yetcites [10] Whelan, 2015, Error, signal, and the placement of Ctenophora sister to all other animals, Proc. Natl. Acad. Sci. USA source

In the paper

“CAT-GTR+G was used by [6]”

What the sources say

• Not checked yetcites [6] Pisani, 2015, Genomic data do not support comb jellies as the sister group to all other animals, Proc. Natl. Acad. Sci. USA source

In the paper

“We conclude that Ctenophora-sister is a tree reconstruction artifact, whereas a placement of the sponges as the sister group of all other animals most likely reflects genuine phylogenetic signal.”

In the paper

“PFschemes were used by [10]”

What the sources say

• Not checked yetcites [10] Whelan, 2015, Error, signal, and the placement of Ctenophora sister to all other animals, Proc. Natl. Acad. Sci. USA source

In the paper

“For each analysis two chains were run and convergence was assessed using the bpcomp and tracecomp tools in PhyloBayes.”

In the paper

“All PPA analyses used a minimum of 100 replicates.”

In the paper

“Amino acid recoding has long been considered as a powerful strategy to reduce compositional heterogeneity and saturation in the data [7, 13-15, 31-36]”

What the sources say

• Not checked yetcites [7] Simion, 2017, A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals, Curr. Biol. source
• Not checked yetcites [13] Hrdy, 2004, Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I, Nature source
• Not checked yetcites [14] Susko, 2007, On reduced amino acid alphabets for phylogenetic inference, Mol. Biol. Evol. source
• Not checked yetcites [15] Kosiol, 2004, A new criterion and method for amino acid classification, J. Theor. Biol. source
• Not checked yetcites [31] Rodríguez-Ezpeleta, 2007, Detecting and overcoming systematic errors in genome-scale phylogenies, Syst. Biol. source
• Not checked yetcites [32] Cox, 2008, The archaebacterial origin of eukaryotes, Proc. Natl. Acad. Sci. USA source
• Not checked yetcites [33] Rota-Stabelli, 2013, Serine codon-usage bias in deep phylogenomics: pancrustacean relationships as a case study, Syst. Biol. source
• Not checked yetcites [34] Domman, 2015, Plastid establishment did not require a chlamydial partner, Nat. Commun. source
• Not checked yetcites [35] Borowiec, 2015, Extracting phylogenetic signal and accounting for bias in whole-genome data sets supports the Ctenophora as sister to remaining Metazoa, BMC Genomics source
• Not checked yetcites [36] Schwentner, 2017, A phylogenomic solution to the origin of insects by resolving crustacean-hexapod relationships, Curr. Biol. source

In the paper

“as the latter was obtained in [10] by removing genes of significant compositional heterogeneity from D16”

What the sources say

• Not checked yetcites [10] Whelan, 2015, Error, signal, and the placement of Ctenophora sister to all other animals, Proc. Natl. Acad. Sci. USA source

In the paper

“Because amino acids are grouped into classes recoding strategies can in some cases cause signal erosion. This however can be monitored because it will result in collapsed nodes that do not provide support for any topology, rather than a change in the topology supported by the data.”

In the paper

“Different sites and lineages accumulate substitutions at different rates (e.g., [67-69])”

What the sources say

• Not checked yetcites [67] Yang, 1993, Maximum-likelihood estimation of phylogeny from DNA sequences when substitution rates differ over sites, Mol. Biol. Evol.
• Not checked yetcites [68] Thorne, 1998, Estimating the rate of evolution of the rate of molecular evolution, Mol. Biol. Evol. source
• Not checked yetcites [69] Yang, 1994, Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods, J. Mol. Evol. source

In the paper

“different amino acids are preferentially found at different sites or in different lineages (e.g., [26, 55])”

What the sources say

• Not checked yetcites [26] Lartillot, 2007, Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model, BMC Evol. Biol. source
• Not checked yetcites [55] Foster, 2004, Modeling compositional heterogeneity, Syst. Biol. source

In the paper

“Because Dayhoff recoding clusters amino acids with comparable properties within the same category, it reduces heterogeneity across both sites and lineages, potentially reducing the impact of systematic errors on phylogenetic estimation under currently available models.”

In the paper

“different proteins can have their own protein-specific replacement rates (e.g., [24])”

What the sources say

• Not checked yetcites [24] Lanfear, 2012, Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses, Mol. Biol. Evol. source

In the paper

“Dayhoff recoding partitions amino acids in six classes or bins (Table 2), based on the log odds matrix of probabilities of pairs of amino acids appearing together in a PAM 250 matrix”

What the sources say

• Not checked yetcites [14] Susko, 2007, On reduced amino acid alphabets for phylogenetic inference, Mol. Biol. Evol. source
• Not checked yetcites [37] Dayhoff, 1978, A model of evolutionary change in proteins