Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 5507 No. 1: 11 Sept. 2024
Type: Article
Published: 2024-09-11
DOI: 10.11646/zootaxa.5507.1.5
Page range: 123-139
Abstract views: 450
PDF downloaded: 196

Expanded distribution and a new genus for rock-inhabiting sea pens (Cnidaria, Anthozoa, Octocorallia, Pennatuloidea)

Department of Biology; University of Louisiana at Lafayette; Louisiana; USA 70504
Department of Biology; University of Louisiana at Lafayette; Louisiana; USA 70504
Octocorallia rock pens Anthoptilidae phylogenetics deep sea Ultra-conserved Elements (UCE) mitogenome

Abstract

Sea pens (Superfamily Pennatuloidea) are a specialized group of octocorals that evolved to live embedded in a soft-sedimented seafloor using their peduncles as anchors. Rock-inhabiting sea pens (“rock pens”) were first described in 2011; their peduncle is modified into a suction cup-like structure that allows them to attach onto the surface of hard substrates, an adaptation previously unknown in sea pens. There are currently four species that have been identified as rock pens based on their peduncular morphology: three of these are in the genus Anthoptilum (Anthoptilidae), and one in the genus Calibelemnon (Scleroptilidae). Herein, we explore the geographic distribution and depth ranges of rock pens using observations from remotely operated vehicles and investigate the evolutionary origins of the rock pens. We present a phylogenomic study of sea pens, based on DNA sequences from hundreds of ultraconserved elements (UCE) and compare these trees to those constructed using mitochondrial gene regions. Our results show that the ancestral sea pen had a typical elongated peduncle. The adaptation to attach onto hard, rocky substrates using the special suction cup-like peduncle evolved along a single derived lineage that is sister to a lineage comprising the genus Anthoptilum. We propose all known rock pen species be grouped into a single new genus, described herein, in the family Anthoptilidae, to reflect the phylogenetic history.

 

References

  1. Aberer, A.J., Kobert, K. & Stamatakis, A. (2014) ExaBayes: Massively Parallel Bayesian Tree Inference for the Whole-Genome Era. Molecular Biology and Evolution, 31 (10), 2553– 2556. https://doi.org/10.1093/molbev/msu236
  2. Alfaro, M.E. & Holder, M.T. (2006) The Posterior and the Prior in Bayesian Phylogenetics. Annual Review of Ecology, Evolution, and Systematics, 37, 19–42. https://doi.org/10.1146/annurev.ecolsys.37.091305.110021
  3. Bankevich, A., Nurk, S., Antipov, D., Gurevich, A.A., Dvorkin, M., Kulikov, A.S., Lesin, V.M., Nikolenko, S.I., Pham, S., Prjibelski, A.D., Pyshkin, A.V., Sirotkin, A.V., Vyahhi, N., Tesler, G., Alekseyev, M.A., Pevzner, P.A., (2012) SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing. Journal of Computational Biology, 19 (5), 455–477. https://doi.org/10.1089/cmb.2012.0021
  4. Brugler, M.R. & France, S.C. (2008) The Mitochondrial Genome of a Deep-Sea Bamboo Coral (Cnidaria, Anthozoa, Octocorallia, Isididae): Genome Structure and Putative Origins of Replication Are Not Conserved Among Octocorals. Journal of Molecular Evolution, 67, 125–136. https://doi.org/10.1007/s00239-008-9116-2
  5. Dierckxsens, N., Mardulyn, P. & Smits, G. (2017) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Research, 45 (4), e18. https://doi.org/10.1093/nar/gkw955
  6. Edgar, R.C. (2004) Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32 (5), 1792–1797. https://doi.org/10.1093/nar/gkh340
  7. Erickson, K.L., Pentico, A., Quattrini, A.M. & McFadden, C.S. (2021) New approaches to species delimitation and population structure of anthozoans: Two case studies of octocorals using ultraconserved elements and exons. Molecular Ecology Resources, 21 (1), 78–92. https://doi.org/10.1111/1755-0998.13241
  8. Faircloth, B.C. (2016) PHYLUCE is a software package for the analysis of conserved genomic loci. Bioinformatics, 32 (5), 786–788. https://doi.org/10.1093/bioinformatics/btv646
  9. France, S.C. & Hoover, L.L. (2002) DNA sequences of the mitochondrial COI gene have low levels of divergence among deep-sea octocorals (Cnidaria: Anthozoa). Hydrobiologia, 471 (1–3), 149–155. https://doi.org/10.1023/A:1016517724749
  10. France, S.C., Rosel, P.E., Agenbroad, J.E., Mullineaux, L.S. & Kocher, T.D. (1996) DNA sequence variation of mitochondrial large-subunit rRNA provides support for a two-subclass organization of the Anthozoa (Cnidaria). Molecular Marine Biology and Biotechnology, 5 (1), 15-28.
  11. Hogan, R.I., Hopkins, K., Wheeler, A.J., Allcock, A.L. & Yesson, C. (2019) Novel diversity in mitochondrial genomes of deep-sea Pennatulacea (Cnidaria: Anthozoa: Octocorallia). Mitochondrial DNA, Part A, 1–14. https://doi.org/10.1080/24701394.2019.1634699
  12. Katoh, K. & Standley, D.M. (2013) MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Molecular Biology and Evolution, 30 (4), 772–780. https://doi.org/10.1093/molbev/mst010
  13. Kennedy, B.R.C., Cantwell, K., Malik, M., Kelley, C., Potter, J., Elliott, K., Lobecker, E., Gray, L.M., Sowers, D., White, M.P., France, S.C., Auscavitch, S., Mah, C., Moriwake, V., Bingo, S.R.D., Putts, M. & Rotjan, R.D. (2019) The Unknown and the Unexplored: Insights Into the Pacific Deep-Sea Following NOAA CAPSTONE expeditions Frontiers in Marine Science, 6, 480. https://doi.org/10.3389/fmars.2019.00480
  14. Kölliker, A. (1880) Report on the Pennatulida dredged by HMS Challenger during the years 1873–1876. Report on the scientific results of the voyage of H.M.S. Challenger during the years 1873–1876. Zoology. Vol. 1. Pt. 2. Her Majesty’s Stationery Office, London, 41 pp.
  15. Kükenthal, W. & Schulze, F.E. (1915) Anthozoa: Pennatularia. In: Das Tierreich. R. Friedländer und Sohn, Berlin, pp. 1–132. https://doi.org/10.5962/bhl.title.1092
  16. Kushida, Y., Kise, H., Iguchi, A., Fujiwara, Y. & Tsuchida, S. (2024) Description of the fifth sea pen species that attaches to hard substrates by modifying its peduncle. Deep Sea Research Part I: Oceanographic Research Papers, 203, 104212. https://doi.org/10.1016/j.dsr.2023.104212
  17. McFadden, C.S., van Ofwegen, L.P. & Quattrini, A.M. (2022) Revisionary systematics of Octocorallia (Cnidaria: Anthozoa) guided by phylogenomics. Bulletin of the Society of Systematic Biologists, 1 (3), 1–79. https://doi.org/10.18061/bssb.v1i3.8735
  18. Miller, M.A., Pfeiffer, W. & Schwartz, T. (2011) The CIPRES science gateway: a community resource for phylogenetic analyses. In: Proceedings of the 2011 TeraGrid Conference: extreme digital discovery, 2011, 1–8. https://doi.org/10.1145/2016741.2016785
  19. Mirarab, S., Reaz, R., Bayzid, M.S., Zimmermann, T., Swenson, M.S. & Warnow, T. (2014) Astral: genome-scale coalescent-based species tree estimation. Bioinformatics, 30 (17), i541–i548. https://doi.org/10.1093/bioinformatics/btu462
  20. Nutting, C.C. (1908) Descriptions of the Alcyonaria collected by the U.S. Bureau of Fisheries steamer Albatross in the vicinity of the Hawaiian Islands in 1902. Proceedings of the United States National Museum, 34, 543–601. https://doi.org/10.5479/si.00963801.34-1624.543
  21. Steel, M. & Penny, D. (2000) Parsimony, Likelihood, and the Role of Models in Molecular Phylogenetics. Molecular Biology and Evolution, 17 (6), 839–850. https://doi.org/10.1093/oxfordjournals.molbev.a026364
  22. Talavera, G. & Castresana, J. (2007) Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments. Systematic Biology, 56 (4), 564–577. https://doi.org/10.1080/10635150701472164
  23. Thomson, J.A., Henderson, W.D. & Simpson, J.J. (1906) An account of the alcyonarians collected by the Royal Indian Marine Survey Ship Investigator in the Indian Ocean. Order of the Trustees of the Indian Museum, Calcutta, xvi + 132 pp., X pls. https://doi.org/10.5962/bhl.title.11622
  24. Verrill, A.E. (1879) Notice of Recent Additions to the Marine Fauna of the Eastern Coast of North America. American Journal of Science, 3 (100), 309–315. https://doi.org/10.2475/ajs.s3-17.100.309
  25. Werle, E., Schneider, C., Renner, M., Völker, M. & Fiehn, W. (1994) Convenient single step, one tube purification of PCR products for direct sequencing. Nucleic Acids Research, 22 (20), 4354–4355. https://doi.org/10.1093/nar/22.20.4354
  26. Williams, G.C. (1990) The Pennatulacea of southern Africa (Coelenterata, Anthozoa). Cape Town. Annals of The South African Museum, 99, 31–119.
  27. Williams, G.C. (1995) Living genera of sea pens (Coelenterata: Octocorallia: Pennatulacea): illustrated key and synopses. Zoological Journal of the Linnean Society, 113 (2), 93–140. https://doi.org/10.1111/j.1096-3642.1995.tb00929.x
  28. Williams, G.C. (2011) The global diversity of sea pens (Cnidaria: Octocorallia: Pennatulacea). PLoS ONE, 6 (7), e22747. https://doi.org/10.1371/journal.pone.0022747
  29. Williams, G.C. & Alderslade, P. (2011) Three new species of pennatulacean octocorals with the ability to attach to rocky substrata (Cnidaria: Anthozoa: Pennatulacea). Zootaxa, 3001 (1), 33–48. https://doi.org/10.11646/zootaxa.3001.1.2