Advertisement

Polar Biology

, Volume 39, Issue 5, pp 897–912 | Cite as

The taxonomic challenge posed by the Antarctic echinoids Abatus bidens and Abatus cavernosus (Schizasteridae, Echinoidea)

  • Bruno David
  • Thomas SaucèdeEmail author
  • Anne Chenuil
  • Emilie Steimetz
  • Chantal De Ridder
Original Paper

Abstract

Cryptic species have been repeatedly described for two decades among the Antarctic fauna, challenging the classic model of Antarctic species with circumpolar distributions and leading to revisit the richness of the Antarctic fauna. No cryptic species had been so far recorded among Antarctic echinoids, which are, however, relatively well diversified in the Southern Ocean. The R/V Polarstern cruise PS81 (ANT XXIX/3) came across populations of Abatus bidens, a schizasterid so far known by few specimens that were found living in sympatry with the species Abatus cavernosus. The species A. cavernosus is reported to have a circum-Antarctic distribution, while A. bidens is only recorded with certainty in South Georgia and at the northern tip of the Antarctic Peninsula. Based on genetic and morphological analyses, our results clearly show that A. bidens and A. cavernosus are two distinct species. The analyzed specimens of A. bidens group together in two haplogroups separated from one another by 2.7 % of nucleotide differences. They are located in the Weddell Sea and in the Bransfield Strait. Specimens of A. cavernosus form one single haplogroup separated from haplogroups of A. bidens by 5 and 3.5 % of nucleotide differences, respectively. The species was collected in the Drake Passage and in the Bransfield Strait. Morphological analyses differentiate A. bidens from A. cavernosus. In contrast, the two genetic groups of A. bidens cannot be differentiated from one another based on morphology alone, suggesting that they may represent a case of cryptic species, common in many Antarctic taxa, but not yet reported in Antarctic echinoids. This needs to be confirmed by complementary analyses of independent genetic markers.

Keywords

Abatus bidens Abatus cavernosus Cryptic species Echinoidea Schizasteridae Southern Ocean 

Notes

Acknowledgments

Samples were collected during the oceanographic campaign PS81–ANT-XXIX/3 of the R/V Polarstern. The authors would like to thank Prof. Dr. Julian Gutt, chief scientist of this campaign, as well as the crew and the scientific staff. Chantal De Ridder was supported by F.R.S-FNRS “short stay abroad” travel grants (Grant Nr. 2013/V3/5/035). This is contribution nr. XX to the vERSO project (www.versoproject.be), funded by the Belgian Science Policy Office (BELSPO, Contract nr. BR/132/A1/vERSO, contribution n° 9). This is a contribution to team BioME of the CNRS laboratory Biogéosciences (UMR 6282).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Aguilée R, Claessen D, Lambert A (2012) Adaptive radiation driven by the interplay of eco-evolutionary and landscape dynamics. Evolution 67(5):1291–1306. doi: 10.1111/evo.12008 PubMedGoogle Scholar
  2. Allcock AL, Strugnell JM (2012) Southern Ocean diversity: new paradigms from molecular ecology. Trends Ecol Evol 27:520–528CrossRefPubMedGoogle Scholar
  3. Allcock AL, Barratt I, Eléaume M, Linse K, Smith PJ, Steinke G, Stevens DW, Norman MD, Strugnell JM (2010) Cryptic speciation and the circumpolarity debate: a case study on endemic Southern Ocean octopuses using the COI barcode of life. Deep Sea Res II 58:242–249CrossRefGoogle Scholar
  4. Baird HP, Miller KJ , Stark JS (2011) Evidence of hidden biodiversity, ongoing speciation and diverse patterns of genetic structure in giant Antarctic amphipods. Mol Ecol 20:3439–3454CrossRefPubMedGoogle Scholar
  5. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefPubMedGoogle Scholar
  6. Bernasconi I (1925) Resultados de la primera expedicion a Tierra del Fuego (1921). Echinodermos. I Equinoideos. Anales Soc Ci Argent 98:3–17Google Scholar
  7. Bernasconi I (1953) Monografia de los equinoideos argentinos. Anales Mus Nac Hist Nat Buenos Aires 2(6):1–58Google Scholar
  8. Bernasconi I (1966) Los equinoideos y asteroideos colectados por el buque oceanografico R/V “Vema”, frente a las costas Argentinas, Uruguayas y sur de Chile. Revista Mus Argent Ci Nat “Bernardino Rivadavia” 9:147–175Google Scholar
  9. Boissin E, Stöhr S, Chenuil A (2011) Did vicariance and adaptation drive cryptic speciation and evolution of brooding in Ophioderma longicauda (Echinodermata: Ophiuroidea), a common atlanto-mediterranean ophiuroid? Mol Ecol 20:4737–4755CrossRefPubMedGoogle Scholar
  10. Chenuil A, Féral JP (2003) Sequences of mitochondrial DNA suggest that Echinocardium cordatum is a complex of several sympatric or hybridizing species. A pilot study. In: Féral JP, David B (eds) Echinoderm Research 2001. Swets & Zeitlinger, Lisse, pp 15–21Google Scholar
  11. Chenuil A, Gault A, Féral JP (2004) Paternity analysis in the Antarctic brooding sea urchin Abatus nimrodi. A pilot study. Polar Biol 27:117–182CrossRefGoogle Scholar
  12. Chenuil A, Egea E, Rocher C, Touzet H, Féral JP (2008) Does hybridization increase evolutionary rates? Data from the 28S-rDNA D8 domain in echinoderms. J Mol Evol 67:539–550CrossRefPubMedGoogle Scholar
  13. Chenuil A, Egea E, Rocher C, Féral JP (2010) Comparing substitution rates in spatangoid sea urchins with putatively different effective sizes, and other echinoderm datasets. In: Harris LG, Böttger SA, Walker CW, Lesser MP (eds) Echinoderms Durham. Balkema, Leiden, pp 159–161Google Scholar
  14. Coppard S, Zigler KS, Lessios HA (2013) Phylogeography of the sand dollar genus Mellita: cryptic speciation along the coasts of the Americas. Mol Phylogenet Evol 69:1033–1042CrossRefPubMedGoogle Scholar
  15. David B, Mooi R (1990) An echinoid that “gives birth”: morphology and systematics of a new Antartic species, Urechinus mortenseni (Echinodermata, Holasteroida). Zoomorphology 110:75–89CrossRefGoogle Scholar
  16. David B, Choné T, Mooi R, De Ridder C (2005a) Antarctic echinoidea. Synopses of the Antarctic Benthos. Koeltz Scientific Books, KönigsteinGoogle Scholar
  17. David B, Choné T, Mooi R, De Ridder C (2005b) Biodiversity of Antarctic echinoids: a comprehensive and interactive database. Sci Mar 69:201–203CrossRefGoogle Scholar
  18. De Broyer C, Danis B et al (2011) How many species in the Southern Ocean? Towards a dynamic inventory of the antarctic marine species. Deep Sea Res II 58:5–17CrossRefGoogle Scholar
  19. Dettai A, Adamowizc SJ, Allcock L, Arango CP, Barnes DKA, Barratt I, Chenuil A, Couloux A et al (2011) DNA Barcoding and molecular systematics of the benthic and demersal organisms of the CEAMARC survey. Polar Sci 5:298–312CrossRefGoogle Scholar
  20. Díaz A, González-Wevar CA, Maturana CA, Palma AT, Poulin E, Gérard K (2012) Restricted geographic distribution and low genetic diversity of the brooding sea urchin Abatus agassizii (Spatangoidea: Schizasteridae) in the South Shetland Islands: a bridgehead population before the spread to the northern Antarctic Peninsula. Rev Chil Hist Nat 85:457–468CrossRefGoogle Scholar
  21. Egea E, Mérigot B, Mahé-Bézac C, Féral JP, Chenuil A (2011) Differential reproductive timing in Echinocardium spp.: the first Mediterranean survey allows inter-oceanic and inter-specific comparisons. C R Biol 334:13–23CrossRefPubMedGoogle Scholar
  22. Egea E, David B, Choné T, Laurin B, Féral JP, Chenuil A (2016) Morphological and genetic analyses reveal a cryptic species complex in the echinoid Echinocardium cordatum and rule out a stabilizing selection explanation. Mol Phylogenet Evol 94:207–220CrossRefPubMedGoogle Scholar
  23. Gutt J (2013) The expedition of the research vessel “Polarstern” to the Antarctic in 2013 (ANT-XXIX/3). Berichte zur Polar- und Meeresforsch 665:1–151Google Scholar
  24. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  25. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological Statistics Software Package for education and data analysis. Pal Elec 4(1):1–9Google Scholar
  26. Held C (2001) No evidence for slow-down of molecular substitution rates at subzero temperatures in Antarctic serolid isopods(Crustacea, Isopoda, Serolidae). Polar Biol 24:497–501CrossRefGoogle Scholar
  27. Held C, Wägele JW (2005) Cryptic speciation in the giant Antarctic isopod Glyptonotus antarcticus (Isopoda: Valvifera: Chaetiliidae). Sci Mar 69(2):175–181Google Scholar
  28. Hemery LG, Eléaume M, Roussel V, Améziane N, Gallut C, Steinke D, Cruaud C, Couloux A, Wilson NG (2012) Comprehensive sampling reveals circumpolarity and sympatry in seven mitochondrial lineages of the Southern Ocean crinoid species Promachocrinus kerguelensis (Echinodermata). Mol Ecol 21:2502–2518CrossRefPubMedGoogle Scholar
  29. Hoareau TB, Boissin E (2010) Design of phylum-specific hybrid primers for DNA barcoding: addressing the need for efficient COI amplification in the Echinodermata. Mol Ecol Res 10:960–967CrossRefGoogle Scholar
  30. Kaiser S, Brandão SN, Brix S, Barnes DKA, Bowden DA, David B, Gutt J et al (2013) Pattern, process and vulnerability of Antarctic and Southern Ocean benthos: a decadal leap in knowledge and understanding. Mar Biol 160:2295–2317CrossRefGoogle Scholar
  31. Koehler R (1912) Echinodermes nouveaux recueillis dans les mers antarctiques par le Pourquoi-pas (astéries, ophiures et échinides). Zool Anz 39:151–163Google Scholar
  32. Koehler R (1926) Echinodermata Echinoidea. Australasian Antarctic expedition 1911–1914. Sci Rep 8:1–134Google Scholar
  33. Krabbe K, Leese F, Mayer C, Tollrian R, Held C (2009) Cryptic mitochondrial lineages in the widespread pycnogonid Colossendeis megalonyx Hoek, 1881 from Antarctic and Subantarctic waters. Polar Biol 33:281–292CrossRefGoogle Scholar
  34. Kroh A (2015) Abatus cavernosus bidens Mortensen, 1910. In: Kroh A, Mooi R (eds) World Echinoidea Database. Accessed through: World Register of Marine SpeciesGoogle Scholar
  35. Lecointre G, Améziane N, Boisselier MC, Bonillo C, Busson F, Causse R, Chenuil A, Couloux A et al (2013) Is the species flock concept operational? The Antarctic Shelf Case. PloS One 8:e68787CrossRefPubMedPubMedCentralGoogle Scholar
  36. Ledoux JB, Tarnowska K, Gérard K, Lhuillier E, Jacquemin B, Veydmann A, Féral JP, Chenuil A (2012) Fine-scale spatial genetic structure in the brooding sea urchin Abatus cordatus suggests vulnerability of the Southern Ocean marine invertebrates facing global change. Polar Biol 35:611–623CrossRefGoogle Scholar
  37. Lessios HA (2011) Speciation genes in free-spawning marine invertebrates. Integr Comp Biol 51:456–465CrossRefPubMedGoogle Scholar
  38. Linse K, Cope T, Lörz AN, Sands C (2007) Is the Scotia Sea a centre of Antarctic marine diversification? Some evidence of cryptic speciation in the circum-Antarctic bivalve Lissarca notorcadensis (Arcoidea: Philobryidae). Polar Biol 30:1059–1068CrossRefGoogle Scholar
  39. Mortensen T (1909) Die Echinoiden der Deutschen Südpolar Expedition 1901-1903. Deutsche Südpolar Expedition. G Reimer, BerlinGoogle Scholar
  40. Mortensen T (1910) The Echinoidea of the Swedish South Polar Expedition. Wissenschaftliche Ergebnisse der Schwedischen Südpolar-Expedition 1901–1903. Lithographisches Institut des Generalstabs, StockholmGoogle Scholar
  41. Mortensen T (1951) A monograph of the Echinoidea. Vol. 5.2 Spatangoida II. Reitzel CA, CopenhagenGoogle Scholar
  42. Néraudeau D, David B, Madon C (1998) Tuberculation in spatangoid fascioles: delineating plausible homologies. Lethaia 31:323–334CrossRefGoogle Scholar
  43. O’Loughlin PM, Paulay G, Davey N, Michonneau F (2011) The Antarctic region as a marine biodiversity hotspot for echinoderms: diversity and diversification of sea cucumbers. Deep Sea Res II 58:264–275CrossRefGoogle Scholar
  44. Pawson DL (1969) Echinoidea. In: Bushnell VC, Hedgpeth JW (eds) Distribution of selected groups of marine invertebrates in water south of 35°S latitude. Antarctic map folio. Am Geogr Soc, New York, p 38–41Google Scholar
  45. Pearse J, Mooi R, Lockhart SJ, Brandt A (2009) Brooding and species diversity in the southern ocean: selection for brooders or speciation within brooding clades? In: Krupnik I, Lang MA, Miller SE (eds) Smithsonian at the poles: contributions to international polar year science. Smithsonian Institution Scholarly Press, Washington, pp 181–196CrossRefGoogle Scholar
  46. Pierrat B, Saucède T, Festeau A, David B (2012) Antarctic, sub-Antarctic and cold temperate echinoid database. ZooKeys 204:47–52. doi: 10.3897/zookeys.204.3134 CrossRefPubMedGoogle Scholar
  47. Poulin E, Féral J-P (1995) Pattern of spatial distribution of a brood-protecting Schizasterid Echinoid, Abatus cordatus, endemic to Kerguelen Islands. Mar Ecol Prog Ser 118:179–186CrossRefGoogle Scholar
  48. Poulin E, Palma AT, Féral J-P (2002) Evolutionary versus ecological success in Antarctic benthic invertebrates. Trends Ecol Evol 17:218–222CrossRefGoogle Scholar
  49. Raupach MJ, Wägele JW (2006) Distinguishing cryptic species in Antarctic Asellota (Crustacea: Isopoda): a preliminary study of mitochondrial DNA in Acanthaspidia drygalskii. Antarct Sci 18:191–198CrossRefGoogle Scholar
  50. Saucède T, Pierrat B, David B (2014) Chapter 5.26 Echinoids. In: De Broyer C, Koubbi P, Griffiths HJ, Raymond B, d’Udekem d’Acoz C et al (eds) Biogeographic atlas of the Southern Ocean. Scientific Committee on Antarctic Research, Cambridge, p 213–220Google Scholar
  51. Schüller M (2011) Evidence for a role of bathymetry and emergence in speciation in the genus Glycera (Glyceridae, Polychaeta) from the deep Eastern Weddell Sea. Polar Biol 34:549–564CrossRefGoogle Scholar
  52. Smith PJ, Steinke D, McMillan PJ, Stewart AL, McVeagh SM, Diaz de Astarloa JM, Welsford D, Ward RD (2011) DNA barcoding highlights a cryptic species of grenadier Macrourus in the Southern Ocean. J Fish Biol 78:355–365CrossRefPubMedGoogle Scholar
  53. Statsoft France (2002) STATISTICA (logiciel d’analyse de données). Versio 6, www.Statsoft.com
  54. Stockley B, Smith AB, Liittlewood T, Lessios HA, Mackenzie-Dodds JA (2005) Phylogenetic relationships of spatangoid sea urchins (Echinoidea): taxon sampling density and congruence between morphological and molecular estimates. Zool Scr 34:447–468CrossRefGoogle Scholar
  55. Thatje S, Hillenbrand C, Larter R (2005) On the origin of Antarctic marine benthic community structure. Trends Ecol Evol 20:534–540CrossRefPubMedGoogle Scholar
  56. Thompson AF, Heywood KJ, Thorpe SE, Renner AHH, Trasvina A (2009) Surface circulation at the tip of the Antarctic Peninsula from drifters. J Phys Oceanogr 39:3–26CrossRefGoogle Scholar
  57. Ward RD, Holmes BH, O’Hara TD (2008) DNA barcoding discriminates echinoderm species. Mol Ecol Res 8:1202–1211CrossRefGoogle Scholar
  58. Wilson NG, Hunter RL, Lockhart SJ, Halanych KM (2007) Multiple lineages and absence of panmixia in the “circumpolar” crinoid Promachocrinus kerguelensis from the Atlantic sector of Antarctica. Mar Biol 152:895–904CrossRefGoogle Scholar
  59. Wilson NG, Maschek A, Baker BJ (2013) A species flock driven by predation? Secondary metabolites support diversification of slugs in Antarctica. PLoS One 8:e80277CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Bruno David
    • 1
    • 4
  • Thomas Saucède
    • 1
    Email author
  • Anne Chenuil
    • 2
  • Emilie Steimetz
    • 1
  • Chantal De Ridder
    • 3
  1. 1.UMR6282 BiogéosciencesCNRS - Université de Bourgogne Franche-ComtéDijonFrance
  2. 2.Institut Méditerranéen de Biodiversité et d’Ecologie marine et continentale, UMR CNRS 7263Aix-Marseille Université, IRDMarseilleFrance
  3. 3.Laboratoire de Biologie Marine (CP 160/15)Université Libre de BruxellesBrusselsBelgium
  4. 4.Muséum National d’Histoire naturelleParisFrance

Personalised recommendations