Letter | Published:

New deep-sea species of Xenoturbella and the position of Xenacoelomorpha

Nature volume 530, pages 9497 (04 February 2016) | Download Citation

Abstract

The discovery of four new Xenoturbella species from deep waters of the eastern Pacific Ocean is reported here. The genus and two nominal species were described from the west coast of Sweden1,2, but their taxonomic placement remains unstable3,4. Limited evidence placed Xenoturbella with molluscs5,6, but the tissues can be contaminated with prey7,8. They were then considered deuterostomes9,10,11,12,13. Further taxon sampling and analysis have grouped Xenoturbella with acoelomorphs (=Xenacoelomorpha) as sister to all other Bilateria (=Nephrozoa)14,15, or placed Xenacoelomorpha inside Deuterostomia with Ambulacraria (Hemichordata + Echinodermata)16. Here we describe four new species of Xenoturbella and reassess those hypotheses. A large species (>20 cm long) was found at cold-water hydrocarbon seeps at 2,890 m depth in Monterey Canyon and at 1,722 m in the Gulf of California (Mexico). A second large species (~10 cm long) also occurred at 1,722 m in the Gulf of California. The third large species (~15 cm long) was found at ~3,700 m depth near a newly discovered carbonate-hosted hydrothermal vent in the Gulf of California. Finally, a small species (~2.5 cm long), found near a whale carcass at 631 m depth in Monterey Submarine Canyon (California), resembles the two nominal species from Sweden. Analysis of whole mitochondrial genomes places the three larger species as a sister clade to the smaller Atlantic and Pacific species. Phylogenomic analyses of transcriptomic sequences support placement of Xenacoelomorpha as sister to Nephrozoa or Protostomia.

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Accessions

Data deposits

Sequence data have been deposited in GenBank; accession numbers can be found in Supplementary Tables 3–5.

References

  1. 1.

    Xenoturbella bocki n.g., n.sp. a peculiar, primitive turbellarian type. Ark. Zool. 1, 11–29 (1949)

  2. 2.

    New light on the enigmatic Xenoturbella (phylum uncertain): ontogeny and phylogeny. Proc. R. Soc. Lond. B 266, 835–841 (1999)

  3. 3.

    Was ist Xenoturbella? Z. Wiss. Zool. 164, 188–198 (1960)

  4. 4.

    What is Xenoturbella? Zool. Lett. 1, 22 (2015)

  5. 5.

    & Xenoturbella’s molluscan relatives... . Nature 390, 31–32 (1997)

  6. 6.

    …and molluscan embryogenesis. Nature 390, 32 (1997)

  7. 7.

    , , , & Xenoturbella is a deuterostome that eats molluscs. Nature 424, 925–928 (2003)

  8. 8.

    et al. Feeding ecology of Xenoturbella bocki (phylum Xenoturbellida) revealed by genetic barcoding. Mol. Ecol. Resour. 8, 18–22 (2008)

  9. 9.

    et al. Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444, 85–88 (2006)

  10. 10.

    , , & Testing the new animal phylogeny: a phylum level molecular analysis of the animal kingdom. Mol. Phylogenet. Evol. 49, 23–31 (2008)

  11. 11.

    et al. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452, 745–749 (2008)

  12. 12.

    , , & The mitochondrial genome structure of Xenoturbella bocki (phylum Xenoturbellida) is ancestral within the deuterostomes. BMC Evol. Biol. 9, 107 (2009)

  13. 13.

    , & Phylogenomic insights into animal evolution. Curr. Biol. 25, R876–R887 (2015)

  14. 14.

    et al. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc. R. Soc. B 276, 4261–4270 (2009)

  15. 15.

    et al.; NISC Comparative Sequencing Program. The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342, 1242592 (2013)

  16. 16.

    et al. Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470, 255–258 (2011)

  17. 17.

    & Eggs and embryos in Xenoturbella (phylum uncertain) are not ingested prey. Dev. Genes Evol. 215, 358–363 (2005)

  18. 18.

    et al. The mitochondrial DNA of Xenoturbella bocki: genomic architecture and phylogenetic analysis. Theory Biosci. 126, 35–42 (2007)

  19. 19.

    , & PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25, 2286–2288 (2009)

  20. 20.

    RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014)

  21. 21.

    , & Automation and evaluation of the SOWH Test with SOWHAT. Syst. Biol. 64, 1048–1058 (2015)

  22. 22.

    & ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31, i44–i52 (2015)

  23. 23.

    , , & Error, signal, and the placement of Ctenophora sister to all other animals. Proc. Natl Acad. Sci. USA 112, 5773–5778 (2015)

  24. 24.

    , , & Animal phylogeny and Its evolutionary implications. Annu. Rev. Ecol. Evol. Syst. 45, 371–395 (2014)

  25. 25.

    et al. Xenacoelomorpha is the sister group to Nephrozoa. Nature (this issue)

  26. 26.

    , & Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proc. Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, LA, 1–8 (IEEE, 2010)

  27. 27.

    & Calyptogena diagonalis, a new vesicomyid bivalve from subduction zone cold seeps in the Eastern North Pacific. Veliger 42, 117–123 (1999)

  28. 28.

    et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012)

  29. 29.

    & Enhancements and modifications of primer design program Primer3. Bioinformatics 23, 1289–1291 (2007)

  30. 30.

    & Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Mol. Biol. Evol. 17, 87–106 (2000)

  31. 31.

    , , , & DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294–299 (1994)

  32. 32.

    , & Complete sequence of the mitochondrial genome of the tapeworm Hymenolepis diminuta: gene arrangements indicate that Platyhelminths are Eutrochozoans. Mol. Biol. Evol. 18, 721–730 (2001)

  33. 33.

    , & TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9, 1657–1659 (2000)

  34. 34.

    & Recent developments in the MAFFT multiple sequence alignment program. Brief. Bioinform. 9, 286–298 (2008)

  35. 35.

    Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540–552 (2000)

  36. 36.

    , & Agalma: an automated phylogenomics workflow. BMC Bioinformatics 14, 330 (2013)

  37. 37.

    et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnol. 29, 644–652 (2011)

  38. 38.

    , & Likelihood-based tests of topologies in phylogenetics. Syst. Biol. 49, 652–670 (2000)

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Acknowledgements

We thank the crew of the R/V Western Flyer and pilots of the ROVs Tiburon and Doc Ricketts for their skill and patience during hunts for these ‘purple socks’. We also thank S. Johnson for verifying bivalve sequences obtained from Xenoturbella and L. Lundsten for hunting through many video files for imagery. We acknowledge the Cyberinfrastructure for Phylogenetic Research (CIPRES) Science Gateway26 for computing resources, and thank M. Miller for additional resources, S. Mirarab for discussions on species tree methods and N. Holland for comments on the manuscript. This work was supported by the David and Lucile Packard Foundation via the Monterey Bay Aquarium Research Institute, Scripps Institution of Oceanography and the National Science Foundation Assembling the Tree of Life program (DEB1036368 to G.W.R.).

Author information

Affiliations

  1. Scripps Institution of Oceanography, University of California, San Diego, La Jolla, California 92037, USA

    • Greg W. Rouse
    • , Nerida G. Wilson
    •  & Jose I. Carvajal
  2. Western Australian Museum, Locked Bag 49, Welshpool DC, Western Australia 6986, Australia

    • Nerida G. Wilson
  3. School of Animal Biology, University of Western Australia, Crawley, Western Australia 6009, Australia

    • Nerida G. Wilson
  4. Monterey Bay Aquarium and Research Institute, Moss Landing, California 95039, USA

    • Robert C. Vrijenhoek

Authors

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Contributions

G.W.R., N.G.W. and R.C.V. collected the specimens. N.G.W. and J.I.C. generated and assembled mitochondrial data for the new Xenoturbella species. J.I.C. generated the Xenoturbella Illumina transcriptome and assembled the data. G.W.R. and J.I.C. performed phylogenetic analyses of mitochondrial genomes and transcriptome data. G.W.R. analysed the morphology of Xenoturbella spp. for the taxonomic descriptions. G.W.R. drafted the paper with J.I.C., N.G.W. and R.C.V. All authors commented on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Greg W. Rouse.

Extended data

Supplementary information

Zip files

  1. 1.

    Supplementary Information

    This zipped file contains Supplementary Tables 1-5 and a Supplementary Table guide.

Videos

  1. 1.

    Clam field at ~3,000 metres depth Monterey Bay, California.

    ROV Tiburon dive 610, October 25, 2004. Collection of a X. monstrosa specimen (type) and images of other Xenoturbella in a field of vesicomyids (mainly Archivesica diagonalis in this clip).

  2. 2.

    Near Pinkie’s Vent at ~1,700 m depth, a cold-water seep in the Guaymas Transform Fault, Gulf of California, Mexico.

    ROV Doc Ricketts dive 385, April 13, 2012. The Mexican paratype of X. monstrosa is shown initially followed by the holotype of X. churro and then the collection of both specimens.

  3. 3.

    Sediment near a hydrothermal vent at ~3,700 metres in the Pescadero Basin, Gulf of California, Mexico.

    ROV Doc Ricketts dive 757, April 24, 2015. The video shows the female paratype of X. profunda gliding over the sediment in an S-pattern amongst polynoid scaleworms, sea anemones and vesicomyid clams. The video is speeded up to x6 times.

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DOI

https://doi.org/10.1038/nature16545

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