Article

Ctenophore relationships and their placement as the sister group to all other animals

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Abstract

Ctenophora, comprising approximately 200 described species, is an important lineage for understanding metazoan evolution and is of great ecological and economic importance. Ctenophore diversity includes species with unique colloblasts used for prey capture, smooth and striated muscles, benthic and pelagic lifestyles, and locomotion with ciliated paddles or muscular propulsion. However, the ancestral states of traits are debated and relationships among many lineages are unresolved. Here, using 27 newly sequenced ctenophore transcriptomes, publicly available data and methods to control systematic error, we establish the placement of Ctenophora as the sister group to all other animals and refine the phylogenetic relationships within ctenophores. Molecular clock analyses suggest modern ctenophore diversity originated approximately 350 million years ago ± 88 million years, conflicting with previous hypotheses, which suggest it originated approximately 65 million years ago. We recover Euplokamis dunlapae—a species with striated muscles—as the sister lineage to other sampled ctenophores. Ancestral state reconstruction shows that the most recent common ancestor of extant ctenophores was pelagic, possessed tentacles, was bioluminescent and did not have separate sexes. Our results imply at least two transitions from a pelagic to benthic lifestyle within Ctenophora, suggesting that such transitions were more common in animal diversification than previously thought.

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Acknowledgements

This work was made possible in part by a grant of high-performance computing resources and technical support from the Alabama Supercomputer Authority and was supported by the United States National Aeronautics and Space Administration (grant NASA-NNX13AJ31G), the National Science Foundation (grants ANT-1043670, ANT-1043745, 1557923, 1548121 and 1645219) and the Ministry of Education of the Russian Federation (#14W03.31.0015). We thank the International SeaKeepers Society, captains and crew of RV Laurence M Gold, RV Capasetic, RV Penny Mae, RV Defiance, RV Basic Explorer, RV Harle of Fleet Miami and RV Miss Phebe II, as well as J. Jacoby for their help with the collection of ctenophores around the globe. A. Kohn helped with laboratory work and data curation. C. Mills helped with species identifications. The findings and conclusions in this paper are those of the authors and do not necessarily represent the views of the United States Fish and Wildlife Service. This is Molette Biology Laboratory contribution 70 and Auburn University Marine Biology Program contribution 166.

Author information

Affiliations

  1. Molette Biology Laboratory for Environmental and Climate Change Studies, Department of Biological Sciences, Auburn University, Auburn, AL, 36849, USA

    • Nathan V. Whelan
    •  & Kenneth M. Halanych
  2. Warm Springs Fish Technology Center, US Fish and Wildlife Service, 5308 Spring St, Warm Springs, GA, 31830, USA

    • Nathan V. Whelan
  3. Department of Biological Sciences, The University of Alabama, Box 870344, Tuscaloosa, AL, 35487, USA

    • Kevin M. Kocot
  4. The Whitney Laboratory for Marine Biosciences, University of Florida, St. Augustine, FL, 32080, USA

    • Tatiana P. Moroz
    • , Krishanu Mukherjee
    • , Peter Williams
    •  & Leonid L. Moroz
  5. Florida Museum of Natural History, University of Florida, Gainesville, FL, 32611, USA

    • Gustav Paulay
  6. Department of Neuroscience and McKnight Brain Institute, University of Florida, Gainesville, FL, 32611, USA

    • Leonid L. Moroz

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Contributions

N.V.W., K.M.K., L.L.M. and K.M.H. designed the study. K.M.K. collected and identified the Australian speices. L.L.M. and G.P. collected and identified all other ctenophores. P.W., K.M., T.P.M. and L.L.M. sequenced and assembled the ctenophore transcriptomes. N.V.W. and K.M.K. performed phylogenetic analyses and ancestral state reconstruction. N.V.W., K.M.K., L.L.M. and K.M.H. wrote the manuscript. All authors edited manuscript versions and approved the final version.

Competing interests

The authors declare no competing financial interests

Corresponding authors

Correspondence to Nathan V. Whelan or Leonid L. Moroz or Kenneth M. Halanych.

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