Deep Genomic-Scale Analyses of the Metazoa Reject Coelomata: Evidence from Single- and Multigene Families Analyzed Under a Supertree and Supermatrix Paradigm
Open accessAbstract
Solving the phylogeny of the animals with bilateral symmetry has proven difficult. Morphological studies have suggested a variety of alternative hypotheses, of which, Hyman's Coelomata hypothesis has become the most established. Studies based on 18S rRNA have failed to endorse Coelomata, supporting instead the rearrangement of the protostomes into two new clades: the Lophotrochozoa (including, e.g., the molluscs and the annelids) and the Ecdysozoa (including the Panarthropoda and most pseudocoelomates, such as the nematodes and priapulids). Support for this new animal phylogeny has been attained from expressed sequence tag studies, although these generally have a limited gene sampling. In contrast, deep genomic-scale analyses have often supported Coelomata. However, these studies are problematic due to their limited taxonomic sampling, which could exacerbate tree reconstruction artifacts. Here, we address both of these sampling limitations; we study the effect of long-branch attraction (LBA) in deep genomic-scale analyses and provide convincing evidence, using both single- and multigene families, that Coelomata is an artifact. We show that optimal outgroup selection is key in avoiding LBA and identify the use of inadequate outgroups as the reason previous deep genomic-scale analyses found strong support for Coelomata.
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The increased difficulty in overcoming LBA in the LEAP dataset compared to LEAN is because platyhelminths are more distantly related to arthropods than nematodes, and hence their shared evolutionary history and the internal branch joining these lineages is shorter.
“This is because although both lineages are fast evolving, platyhelminths (LEAP) are more distantly related to arthropods than nematodes (LEAN), and hence their shared evolutionary history, and the internal branch joining these lineages, is shorter57,58.”
From Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding (2021) · cites this paper as [58]
The Results (Four-Taxon Data Sets; page unavailable) place a nematode as the sister group of an arthropod and discuss long-branch attraction. The paper does not compare LEAP with LEAN or attribute a shorter shared history or internal branch to platyhelminths’ relationship with arthropods, so it does not support the proposed explanation for the difference between those datasets. (LLM, conf=0.83)
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“Although lack of unambiguous morphological support for Ecdysozoa persists as a moot point, in the light of overwhelming molecular evidence and lack of morphological evidence conclusively discrediting Ecdysozoa, is it now finally time to shed the notion of Coelomata?”
BackgroundMethodResultInfluentialSelf-citationDoes a tree–like phylogeny only exist at the tips in the prokaryotes?
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Pisani, D. (2004) · Systematic Biology · doi:10.1080/10635150490888877 · Cited by 107 · cited 4× · see citing works
“…sampling (see also Halanych 2004), which can exacerbate phylogenetic artifacts, particularly long-branch attraction (LBA), in the presence of a fast-evolving species such as C. elegans (e.g., Pisani 2004; Delsuc et al. 2005; Philippe et al. 2005; Jeffroy et al. 2006; Sperling et al. 2009).”
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Self-citation
- Authors
- Holton, T. A., & Pisani, D.
- Affiliations
- National University of Ireland, Maynooth (IE)
- Corresponding author
- Holton, Thérèse A.
- Venue
- Genome Biology and Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-01-01
- Volume
- 2
- Pages
- 310-324
- ISSN
- 1759-6653 (ISSN-L)
- PMC
- PMC2997542
- OpenAlex
- W2162552502
- Cited by
- 51
- References
- 9
- Citations by year
- 2023: 1 · 2022: 5 · 2021: 2 · 2020: 3 · 2017: 1 · 2016: 2 · 2015: 2 · 2014: 4 · 2013: 10 · 2012: 13
- FWCI
- 4.04
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by-nc
- Locations
- Genome Biology and Evolution (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Explore Bristol Research (publishedVersion)
- Bristol Research (University of Bristol) (submittedVersion)
- Funders
- Irish Research Council for Science, Engineering and Technology
- Science Foundation Ireland
- Irish Centre for High-End Computing
- 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 › Invertebrate Taxonomy and Ecology
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Keywords
- animal phylogeny, animals, long-branch attraction, outgroup selection, Lophotrochozoa, Ecdysozoa, gene family, supertree, supermatrix, taxon sampling, 18S rRNA phylogeny
- MeSH terms
- Animals, Bayes Theorem, Multigene Family, Invertebrates, Models, Genetic, Phylogeny, Proteins, Evolution, Molecular, Genomics, Databases, Genetic, Eukaryota
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