Improved Phylogenomic Taxon Sampling Noticeably Affects Nonbilaterian Relationships

Department of Earth- and Environmental Sciences, Palaeontology and Geobiology & GeoBio-Center, Ludwig-Maximilians-Universität München, Richard-Wagner-Str. 10, 80333 München, Germany.
Molecular Biology and Evolution (Impact Factor: 9.11). 04/2010; 27(9):1983-7. DOI: 10.1093/molbev/msq089
Source: PubMed

ABSTRACT Despite expanding data sets and advances in phylogenomic methods, deep-level metazoan relationships remain highly controversial. Recent phylogenomic analyses depart from classical concepts in recovering ctenophores as the earliest branching metazoan taxon and propose a sister-group relationship between sponges and cnidarians (e.g., Dunn CW, Hejnol A, Matus DQ, et al. (18 co-authors). 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745-749). Here, we argue that these results are artifacts stemming from insufficient taxon sampling and long-branch attraction (LBA). By increasing taxon sampling from previously unsampled nonbilaterians and using an identical gene set to that reported by Dunn et al., we recover monophyletic Porifera as the sister group to all other Metazoa. This suggests that the basal position of the fast-evolving Ctenophora proposed by Dunn et al. was due to LBA and that broad taxon sampling is of fundamental importance to metazoan phylogenomic analyses. Additionally, saturation in the Dunn et al. character set is comparatively high, possibly contributing to the poor support for some nonbilaterian nodes.

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Available from: Gert Wörheide, Sep 28, 2015
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    • "tationally intensive for some phylogenomic datasets ( e . g . , Nesnidal et al . 2010 , Ryan et al . 2013 ; Moroz et al . 2014 ) . Generally , Bayesian analyses using the CAT model , which has been shown to suppress LBA artifacts ( Latrillot et al . 2007 ) , have recovered sponges as sister to all remaining animals ( Philippe et al . 2009 , 2011 ; Pick et al . 2010 ; Nosenko et al . 2013 , but see Borowiec et al . 2015 ; Whelan et al . 2015 ) . A sister relationship between cnidarians and ctenophores has only been recovered in analyses that used the CAT model on datasets dominated by ribosomal protein genes ( Philippe et al . 2009 ; Nosenko et al . 2013 ) , and Whelan et al . ( 2015 ) showed ribos"
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    ABSTRACT: Despite an explosion in the amount of sequence data, phylogenomics has failed to settle controversy regarding some critical nodes on the animal tree of life. Understanding relationships among Bilateria, Ctenophora, Cnidaria, Placozoa, and Porifera is essential for studying how complex traits such as neurons, muscles, and gastrulation have evolved. Recent studies have cast doubt on the historical viewpoint that sponges are sister to all other animal lineages with recent studies recovering ctenophores as sister. However, the ctenophore-sister hypothesis has been criticized as unrealistic and caused by systematic error. We review past phylogenomic studies and potential causes of systematic error in an effort to identify areas that can be improved in future studies. Increased sampling of taxa, less missing data, and a priori removal of sequences and taxa that may cause systematic error in phylogenomic inference will likely be the most fruitful areas of focus when assembling future datasets. Ultimately, we foresee metazoan relationships being resolved with higher support in the near future, and we caution against dismissing novel hypotheses merely because they conflict with historical viewpoints of animal evolution. © The Author 2015. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email:
    Integrative and Comparative Biology 05/2015; DOI:10.1093/icb/icv037 · 2.93 Impact Factor
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    • "Regardless of the position of Ctenophora, we suggest that the most likely position of Dendrogramma is before Bilateria, being related to either Ctenophora and/or Cnidaria based on the general similarities in body organisation (e.g., presence of mesoglea and gastrovascular system). If indeed Porifera is the sister group to the remaining metazoans as traditionally perceived and recently supported by a re-analysis [10], [11] of a major molecular dataset from [6], [7], and if Ctenophora and Cnidaria are sister taxa ( = Coelenterata), as was the result of the same re-analysis [10], [11], then Dendrogramma may be related to Coelenterata. "
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    ABSTRACT: A new genus, Dendrogramma, with two new species of multicellular, non-bilaterian, mesogleal animals with some bilateral aspects, D. enigmatica and D. discoides, are described from the south-east Australian bathyal (400 and 1000 metres depth). A new family, Dendrogrammatidae, is established for Dendrogramma. These mushroom-shaped organisms cannot be referred to either of the two phyla Ctenophora or Cnidaria at present, because they lack any specialised characters of these taxa. Resolving the phylogenetic position of Dendrogramma depends much on how the basal metazoan lineages (Ctenophora, Porifera, Placozoa, Cnidaria, and Bilateria) are related to each other, a question still under debate. At least Dendrogramma must have branched off before Bilateria and is possibly related to Ctenophora and/or Cnidaria. Dendrogramma, therefore, is referred to Metazoa incertae sedis. The specimens were fixed in neutral formaldehyde and stored in 80% ethanol and are not suitable for molecular analysis. We recommend, therefore, that attempts be made to secure new material for further study. Finally similarities between Dendrogramma and a group of Ediacaran (Vendian) medusoids are discussed.
    PLoS ONE 09/2014; 9(9):1-11. DOI:10.1371/journal.pone.0102976 · 3.23 Impact Factor
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    • "Resolving the Tree of Life has been prioritized as one of the 125 most important unsolved scientific questions in 2005 by Science (Kennedy 2005), and the advent of phylogenomics has aided in resolving many contentious aspects in animal phylogeny (e.g., Philippe and Telford 2006; Dunn et al. 2008; Bleidorn et al. 2009; Hejnol et al. 2009; Meusemann et al. 2010; Kocot et al. 2011; Rehm et al. 2011; Smith et al. 2011; Struck et al. 2011; Hartmann et al. 2012; von Reumont et al. 2012). This is not without controversy, and several phenomena unique to genome-scale data have been identified as negatively impacting tree reconstruction in this paradigm, perhaps foremost among these being gene occupancy (missing data) (Roure et al. 2013; Dell'Ampio et al. 2014), taxon sampling (Pick et al. 2010), and quality of data (e.g., proper ortholog assignment and controls on exogenous contamination ) (Philippe et al. 2011; Salichos and Rokas 2011). In addition , assumptions underlying concatenation (Salichos and Rokas 2013) and model (mis-)specification (Lartillot and Philippe 2008) have also been identified as possible pitfalls for tree reconstruction in a phylogenomic framework. "
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    ABSTRACT: Relationships between the five extant orders of centipedes have been considered solved based on morphology. Phylogenies based on samples of up to a few dozen genes have largely been congruent with the morphological tree apart from an alternative placement of one order, the relictual Craterostigmomorpha, consisting of two species in Tasmania and New Zealand. To address this incongruence, novel transcriptomic data were generated to sample all five orders of centipedes, and also used as a test case for studying gene-tree incongruence. Maximum likelihood and Bayesian mixture model analyses of a dataset composed of 1934 orthologues with 45% missing data, as well as the 389 orthologues in the least saturated, stationary quartile, retrieve strong support for a sister group relationship between Craterostigmomorpha and all other pleurostigmophoran centipedes, of which the latter group is newly named Amalpighiata. The Amalpighiata hypothesis, which shows little gene-tree incongruence and is robust to the influence of among-taxon compositional heterogeneity, implies convergent evolution in several morphological and behavioral characters traditionally used in centipede phylogenetics, such as maternal brood care, but accords with patterns of first appearances in the fossil record.
    Molecular Biology and Evolution 03/2014; 31(6). DOI:10.1093/molbev/msu108 · 9.11 Impact Factor
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