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


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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    • "Cnidarians ( jellyfish, corals, sea anemones) are the sister clade of the Bilateria (Hejnol et al., 2009; Pick et al., 2010), and they possess simple, nerve-net based nervous systems comprising three classes of neural cells – sensory neurons, ganglion neurons (analogous to interneurons) and nematocytes (mechano-/chemoreceptor cells). Due to their relative phylogenetic positions, identifying conserved features of cnidarian and bilaterian neurogenesis can inform reconstructions of the ancestral neurogenic characters of eumetazoans (herein referring to Bilateria+Cnidaria). Indeed, genomic comparisons have shown that cnidarians possess many orthologues to key bilaterian neural-related genes (Chapman et al., 2010; Galliot et al., 2009; Putnam et al., 2007; Watanabe et al., 2009), but a functional characterisation of the majority of these candidates is lacking. "
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    ABSTRACT: Notch signalling, SoxB and Group A bHLH 'proneural' genes are conserved regulators of the neurogenic program in many bilaterians. However, the ancestry of their functions and interactions is not well understood. We address this question in the sea anemone Nematostella vectensis, a representative of the Cnidaria, the sister clade to the Bilateria. It has previously been found that the SoxB orthologue NvSoxB(2) is expressed in neural progenitor cells (NPCs) in Nematostella and promotes the development of both neurons and nematocytes, whereas Notch signalling has been implicated in the negative regulation of neurons and the positive regulation of nematocytes. Here, we clarify the role of Notch by reporting that inhibition of Notch signalling increases the numbers of both neurons and nematocytes, as well as increasing the number of NvSoxB(2)-expressing cells. This suggests that Notch restricts neurogenesis by limiting the generation of NPCs. We then characterise NvAth-like (Atonal/Neurogenin family) as a positive regulator of neurogenesis that is co-expressed with NvSoxB(2) in a subset of dividing NPCs, while we find that NvAshA (Achaete-scute family) and NvSoxB(2) are co-expressed in non-dividing cells only. Reciprocal knockdown experiments reveal a mutual requirement for NvSoxB(2) and NvAth-like in neural differentiation; however, the primary expression of each gene is independent of the other. Together, these data demonstrate that Notch signalling and NvSoxB(2) regulate Nematostella neural progenitors via parallel yet interacting mechanisms; with different aspects of these interactions being shared with Drosophila and/or vertebrate neurogenesis.
    Development 10/2015; 142(142):3332-3342. DOI:10.1242/dev.123745 · 6.46 Impact Factor
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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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    • "These results further demonstrate that reducing the effects of LBA remains critical, especially in the phylogenomics era (Heath et al. 2008; Hejnol et al. 2009; Pick et al. 2010). Thus, it remains essential to improve taxon sampling to reduce long branches when possible. "
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    ABSTRACT: It is well known that species with elevated substitution rates can give rise to disproportionately long branches in the species tree. This combination of long and short branches can contribute to long-branch artifacts (LBA). Despite efforts to remedy LBA via increased taxon sampling and methodological improvements in gene tree estimation, it remains unclear how long and short branches affect species tree estimation in the presence of incomplete lineage sorting (ILS). Here, we examine the combined influence of long external and short internal branches on concatenation and coalescent methods using both simulated and empirical data. Our results demonstrate that the presence of long and short branches alone does not obviously confound the consistency of concatenation and coalescent methods. However, when long external and short internal branches occur simultaneously with high ILS, concatenation methods can be misled, especially when two of these long branches are sister lineages. In contrast, coalescent methods are more robust under these circumstances. This is particularly relevant because this topological pattern also characterizes numerous ancient rapid radiations across the Tree of Life. Since short internal branches can increase the potential for ILS and gene tree discordance, our results collectively suggest that coalescent methods are more likely to infer the correct species tree in cases of ancient rapid radiations where long external and short internal branches are in close phylogenetic proximity. © The Author 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail:
    Molecular Biology and Evolution 11/2014; 32(3). DOI:10.1093/molbev/msu331 · 9.11 Impact Factor
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