Support for a clade of Placozoa and Cnidaria in genes with minimal compositional bias

  1. Christopher E Laumer  Is a corresponding author
  2. Harald Gruber-Vodicka
  3. Michael G Hadfield
  4. Vicki B Pearse
  5. Ana Riesgo
  6. John C Marioni
  7. Gonzalo Giribet
  1. Wellcome Trust Sanger Institute, United Kingdom
  2. Max Planck Institute for Marine Microbiology, Germany
  3. University of Hawaii at Manoa, United States
  4. University of California, Santa Cruz, United States
  5. The Natural History Museum, United Kingdom
  6. Harvard University, United States

Abstract

The phylogenetic placement of the morphologically simple placozoans is crucial to understanding the evolution of complex animal traits. Here, we examine the influence of adding new genomes from placozoans to a large dataset designed to study the deepest splits in the animal phylogeny. Using site-heterogeneous substitution models, we show that it is possible to obtain strong support, in both amino acid and reduced-alphabet matrices, for either a sister-group relationship between Cnidaria and Placozoa, or for Cnidaria and Bilateria as seen in most published work to date, depending on the orthologues selected to construct the matrix. We demonstrate that a majority of genes show evidence of compositional heterogeneity, and that support for the Cnidaria+Bilateria clade can be assigned to this source of systematic error. In interpreting these results, we caution against a peremptory reading of placozoans as secondarily reduced forms of little relevance to broader discussions of early animal evolution.

Data availability

SRA accession codes, where used, and all alternative sources for sequence data (e.g. individually hosted websites, personal communications), are listed above in the Materials and Methods section. A DataDryad accession is available at https://doi.org/10.5061/dryad.6cm1166, which makes available all helper scripts, orthogroups, multiple sequence alignments, phylogenetic program output, and raw host proteomes inputted to OrthoFinder. Metagenomic bins containing placozoan host contigs and raw RNA reads used to derive gene annotations from H4, H6 and H11 isolates are also provided in this accession. PhyloBayes .chain files, due to their large size, are separately accessioned at in Zenodo at https://doi.org/10.5281/zenodo.1197272.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Christopher E Laumer

    Wellcome Trust Sanger Institute, Hinxton, United Kingdom
    For correspondence
    claumer@ebi.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8097-8516
  2. Harald Gruber-Vodicka

    Max Planck Institute for Marine Microbiology, Bremen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Michael G Hadfield

    Kewalo Marine Laboratory, Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Vicki B Pearse

    Institute of Marine Sciences, University of California, Santa Cruz, Santa Cruz, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Ana Riesgo

    Life Sciences, Invertebrate Division, The Natural History Museum, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. John C Marioni

    Wellcome Trust Sanger Institute, Hinxton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9092-0852
  7. Gonzalo Giribet

    Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

Max-Planck-Institute fuer Marine Microbiologie

  • Harald Gruber-Vodicka

EMBL-European Bioinformatics Institute

  • John C Marioni

Harvard University Faculty of Arts and Sciences

  • Gonzalo Giribet

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2018, Laumer et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 5,349
    views
  • 740
    downloads
  • 93
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Christopher E Laumer
  2. Harald Gruber-Vodicka
  3. Michael G Hadfield
  4. Vicki B Pearse
  5. Ana Riesgo
  6. John C Marioni
  7. Gonzalo Giribet
(2018)
Support for a clade of Placozoa and Cnidaria in genes with minimal compositional bias
eLife 7:e36278.
https://doi.org/10.7554/eLife.36278

Share this article

https://doi.org/10.7554/eLife.36278

Further reading

    1. Evolutionary Biology
    Mauna R Dasari, Kimberly E Roche ... Elizabeth A Archie
    Research Article

    Mammalian gut microbiomes are highly dynamic communities that shape and are shaped by host aging, including age-related changes to host immunity, metabolism, and behavior. As such, gut microbial composition may provide valuable information on host biological age. Here, we test this idea by creating a microbiome-based age predictor using 13,563 gut microbial profiles from 479 wild baboons collected over 14 years. The resulting ‘microbiome clock’ predicts host chronological age. Deviations from the clock’s predictions are linked to some demographic and socio-environmental factors that predict baboon health and survival: animals who appear old-for-age tend to be male, sampled in the dry season (for females), and have high social status (both sexes). However, an individual’s ‘microbiome age’ does not predict the attainment of developmental milestones or lifespan. Hence, in our host population, gut microbiome age largely reflects current, as opposed to past, social and environmental conditions, and does not predict the pace of host development or host mortality risk. We add to a growing understanding of how age is reflected in different host phenotypes and what forces modify biological age in primates.

    1. Evolutionary Biology
    Julia D Sigwart, Yunlong Li ... Jin Sun
    Research Article

    A major question in animal evolution is how genotypic and phenotypic changes are related, and another is when and whether ancient gene order is conserved in living clades. Chitons, the molluscan class Polyplacophora, retain a body plan and general morphology apparently little changed since the Palaeozoic. We present a comparative analysis of five reference quality genomes, including four de novo assemblies, covering all major chiton clades, and an updated phylogeny for the phylum. We constructed 20 ancient molluscan linkage groups (MLGs) and show that these are relatively conserved in bivalve karyotypes, but in chitons they are subject to re-ordering, rearrangement, fusion, or partial duplication and vary even between congeneric species. The largest number of novel fusions is in the most plesiomorphic clade Lepidopleurida, and the chitonid Liolophura japonica has a partial genome duplication, extending the occurrence of large-scale gene duplication within Mollusca. The extreme and dynamic genome rearrangements in this class stands in contrast to most other animals, demonstrating that chitons have overcome evolutionary constraints acting on other animal groups. The apparently conservative phenome of chitons belies rapid and extensive changes in genome.