Polar Biology

, Volume 39, Issue 4, pp 677–688 | Cite as

Diversity and distribution within the sea spider genus Pallenopsis (Chelicerata: Pycnogonida) in the Western Antarctic as revealed by mitochondrial DNA

  • Avril M. Harder
  • Kenneth M. Halanych
  • Andrew R. MahonEmail author
Original Paper


Pycnogonids are marine arthropods with cosmopolitan and eurybathic distribution. Of the approximately 1300 pycnogonid species described worldwide, over 260 species occur in the Southern Ocean, and over half of those are endemic to the Antarctic. Morphological data suggest circumpolar distributions for multiple Antarctic species; however, recent molecular inquiries into the genetic structure of Antarctic benthic invertebrate populations have revealed varying patterns of genetic connectivity and, in many cases, radiation of morphologically cryptic species incompatible with the previously hypothesized genetic homogeneity for Southern Ocean invertebrates. To date, little is known about genetic connectivity within Antarctic Pallenopsis species populations, and Pallenopsis phylogeny remains poorly resolved. This study describes genetic structure of Pallenopsis populations of western Antarctic coastal regions, the Scotia Arc, Falkland Islands, and Chilean coast. We present the results of analyses derived from the mitochondrial COI gene that demonstrate patterns of connectivity for these populations. Examination of genetic characters has allowed for the identification of divergent mitochondrial lineages within Pallenopsis and will lead to a description of at least one new species. Future sampling and analyses from other areas of the Antarctic coastline will provide a broader context for the phylogeny of Pallenopsis.


Sea spiders Phylogenetics Southern ocean Pallenopsidae 



We thank the staff and crew of the ASRV Laurence M. Gould and the RVIB Nathaniel B. Palmer and the Antarctic Support Company.  This work was supported by National Science Foundation Grants (ANT-1043745, PLR-1043670).  Additionally, this work represents contribution #136 to the AU Marine Biology Program and is contribution #44 to the AU Molette Lab.


  1. Allcock AL, Barratt I, Eléaume M et al (2011) Cryptic speciation and the circumpolarity debate: a case study on endemic Southern Ocean octopuses using the COI barcode of life. Deep Sea Res II 58:242–249. doi: 10.1016/j.dsr2.2010.05.016 CrossRefGoogle Scholar
  2. Arabi J, Cruaud C, Couloux A, Hassanin A (2010) Studying sources of incongruence in arthropod molecular phylogenies: sea spiders (Pycnogonida) as a case study. CR Biol 333:438–453. doi: 10.1016/j.crvi.2010.01.018 CrossRefGoogle Scholar
  3. Arango CP, Wheeler WC (2007) Phylogeny of the sea spiders (Arthropoda, Pycnogonida) based on direct optimization of six loci and morphology. Cladistics 23:255–293. doi: 10.1111/j.1096-0031.2007.00143.x CrossRefGoogle Scholar
  4. Arango CP, Soler-Membrives A, Miller KJ (2011) Genetic differentiation in the circum-Antarctic sea spider Nymphon australe (Pycnogonida: Nymphonidae). Deep Sea Res II 58:212–219. doi: 10.1016/j.dsr2.2010.05.019 CrossRefGoogle Scholar
  5. Arnaud F, Bamber RN (1987) The biology of Pycnogonida. Adv Mar Biol 24:1–96CrossRefGoogle Scholar
  6. Arntz WE, Brey T, Gallardo VA (1994) Antarctic zoobenthos. Oceanogr Mar Biol Annu Rev 32:241–304Google Scholar
  7. Arntz WE, Brey T, Gallardo VA (1997) Antarctic marine biodiversity: an overview. In: Battaglia B, Valencia J, Walton DWH (eds) Antarctic communities: species, structure and survival. Cambridge University Press, Cambridge, pp 3–14Google Scholar
  8. 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 20:3439–3454. doi: 10.1111/j.1365-294X.2011.05173.x CrossRefPubMedGoogle Scholar
  9. Barrett RDH, Hebert PDN (2005) Identifying spiders through DNA barcodes. Can J Zool 83:481–491. doi: 10.1139/z05-024 CrossRefGoogle Scholar
  10. Brey T, Dahm C, Gorny M et al (1996) Do Antarctic benthic invertebrates show an extended level of eurybathy? Antarct Sci 8:3–6CrossRefGoogle Scholar
  11. Child CA (1995) Nymphonidae, Colossendeidae, Rhynchothoracidae, Pycnogonidae, Endeididae, and Callipallenidae. American Geophysical Union, WashingtonCrossRefGoogle Scholar
  12. Clark PU, Dyke AS, Shakun JD et al (2009) The last glacial maximum. Science 325:710–714CrossRefPubMedGoogle Scholar
  13. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660CrossRefPubMedGoogle Scholar
  14. Convey P, Stevens MI, Hodgson DA et al (2009) Exploring biological constraints on the glacial history of Antarctica. Quatern Sci Rev 28:3035–3048. doi: 10.1016/j.quascirev.2009.08.015 CrossRefGoogle Scholar
  15. Dietz L, Krapp F, Hendrickx ME et al (2013) Evidence from morphological and genetic data confirms that Colossendeis tenera Hilton, 1943 (Arthropoda: Pycnogonida), does not belong to the Colossendeis megalonyx Hoek, 1881 complex. Org Divers Evol 13:151–162. doi: 10.1007/s13127-012-0120-4 CrossRefGoogle Scholar
  16. Dietz L, Pieper S, Seefeldt MA, Leese F (2015a) Morphological and genetic data clarify the taxonomic status of Colossendeis robusta and C. glacialis (Pycnogonida) and reveal overlooked diversity. Arthropod Syst Phylogeny 73:107–128Google Scholar
  17. Dietz L, Arango, CP, Domel JS, Halanych KM, Harder AM, Held C, Mahon AR, Mayer C, Melzer RR, Rouse GW, Weis A, Wilson NG, Leese F (2015b) Regional differentiation and extensive hybridization between mitochondrial clades of the Southern Ocean giant sea spider Colossendeis megalonyx. R Soc Open Sci 2: 140424.
  18. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973. doi: 10.1093/molbev/mss075 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Folmer O, Black M, Hoeh W et al (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–299Google Scholar
  20. Fraser CI, Nikula R, Waters JM (2010) Oceanic rafting by a coastal community. Proc R Soc B Biol Sci 278:649–655. doi: 10.1126/science.87.2250.119 CrossRefGoogle Scholar
  21. Fu Y-X (1996) New statistical tests of neutrality for DNA samples from a population. Genetics 143:557–570PubMedPubMedCentralGoogle Scholar
  22. Griffiths HJ, Barnes DKA, Linse K (2009) Towards a generalized biogeography of the Southern Ocean benthos. J Biogeogr 36:162–177. doi: 10.1111/j.1365-2699.2008.01979.x CrossRefGoogle Scholar
  23. 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
  24. Hart MW, Sunday J (2007) Things fall apart: biological species form unconnected parsimony networks. Biol Lett 3:509–512. doi: 10.1098/rsbl.2007.0307 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Havermans C, Nagy ZT, Sonet G et al (2011) DNA barcoding reveals new insights into the diversity of Antarctic species of Orchomene sensu lato (Crustacea: Amphipoda: Lysianassoidea). Deep Sea Res II 58:230–241. doi: 10.1016/j.dsr2.2010.09.028 CrossRefGoogle Scholar
  26. Held C (2003) Molecular evidence for cryptic speciation within the widespread Antarctic crustacean Ceratoserolis trilobitoides (Crustacea, Isopoda). In: Huiskies AHL, Giekes WWW, Rozema J et al (eds) Antarctic biology in a global context. Backhuys, Leiden, pp 135–139Google Scholar
  27. Held C, Wägele J-W (2005) Cryptic speciation in the giant Antarctic isopod Glyptonotus antarcticus (Isopoda: Valvifera: Chaetiliidae). Sci Mar 69:175–181CrossRefGoogle Scholar
  28. Hunter RL, Halanych KM (2010) Phylogeography of the Antarctic planktotrophic brittle star Ophionotus victoriae reveals genetic structure inconsistent with early life history. Mar Biol 157:1693–1704. doi: 10.1007/s00227-010-1443-3 CrossRefGoogle Scholar
  29. Krabbe K, Leese F, Mayer C et al (2010) Cryptic mitochondrial lineages in the widespread pycnogonid Colossendeis megalonyx Hoek, 1881 from Antarctic and Subantarctic waters. Polar Biol 33:281–292. doi: 10.1007/s00300-009-0703-5 CrossRefGoogle Scholar
  30. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi: 10.1093/bioinformatics/btp187 CrossRefPubMedGoogle Scholar
  31. Linse K, Cope T, Lörz A-N, 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 30:1059–1068. doi: 10.1007/s00300-007-0265-3 CrossRefGoogle Scholar
  32. Mahon AR, Arango CP, Halanych KM (2008) Genetic diversity of Nymphon (Arthropoda: Pycnogonida: Nymphonidae) along the Antarctic Peninsula with a focus on Nymphon australe Hodgson 1902. Mar Biol 155:315–323. doi: 10.1007/s00227-008-1029-5 CrossRefGoogle Scholar
  33. Milne I, Lindner D, Bayer M et al (2008) TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 25:126–127. doi: 10.1093/bioinformatics/btn575 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Munilla T, Soler-Membrives A (2009) Check-list of the pycnogonids from Antarctic and sub-Antarctic waters: zoogeographic implications. Antarct Sci 21:99–111. doi: 10.1017/S095410200800151X CrossRefGoogle Scholar
  35. Nielsen JF, Lavery S, Lörz A (2009) Synopsis of a new collection of sea spiders (Arthopoda: Pycnogonida) from the Ross Sea, Antarctica. Polar Biol 32:1147–1155CrossRefGoogle Scholar
  36. Poulin E, Féral JP (1996) Why are there so many species of brooding Antarctic echinoids? Zool Reihe 50:820–830Google Scholar
  37. Prendini L, Weygoldt P, Wheeler WC (2005) Systematics of the group of African whip spiders (Chelicerata: Amblypygi): evidence from behaviour, morphology and DNA. Org Divers Evol 5:203–236. doi: 10.1016/j.ode.2004.12.004 CrossRefGoogle Scholar
  38. Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol Ecol 21:1864–1877. doi: 10.1111/j.1365-294X.2011.05239.x CrossRefPubMedGoogle Scholar
  39. Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6, Available from
  40. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100CrossRefPubMedGoogle Scholar
  41. Raupach MJ, Wägele J-W (2006) Distinguishing cryptic species in Antarctic Asellota (Crustacea: Isopoda)—a preliminary study of mitochondrial DNA in Acanthaspidia drygalskii. Antarct Sci 18:191. doi: 10.1017/S0954102006000228 CrossRefGoogle Scholar
  42. Reid NM, Carstens BC (2012) Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model. BMC Evol Biol 12:196. doi: 10.1186/1471-2148-12-196 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Ronquist F, Teslenko M, van der Mark P et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi: 10.1093/sysbio/sys029 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Scher HD, Martin EE (2006) Timing and climatic consequences of the opening of Drake Passage. Science 312:428–430. doi: 10.1126/science.1120044 CrossRefPubMedGoogle Scholar
  45. Simonsen KL, Churchill GA, Aquadro CF (1995) Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141:413–429PubMedPubMedCentralGoogle Scholar
  46. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. doi: 10.1093/bioinformatics/btu033/-/DC1 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Tajima F (1989) Statistical methods for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  48. Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi: 10.1093/molbev/msr121 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Thatje S, Hillenbrand C-D, Larter R (2005) On the origin of Antarctic marine benthic community structure. Trends Ecol Evol 20:534–540. doi: 10.1016/j.tree.2005.07.010 CrossRefPubMedGoogle Scholar
  50. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefPubMedPubMedCentralGoogle Scholar
  51. Thornhill DJ, Mahon AR, Norenburg JL, Halanych KM (2008) Open-ocean barriers to dispersal: a test case with the Antarctic Polar Front and the ribbon worm Parborlasia corrugatus (Nemertea: Lineidae). Mol Ecol 17:5104–5117. doi: 10.1111/j.1365-294X.2008.03970.x CrossRefPubMedGoogle Scholar
  52. Waters JM (2008) Driven by the West Wind Drift? A synthesis of southern temperate marine biogeography, with new directions for dispersalism. J Biogeogr 35:417–427. doi: 10.1111/j.1365-2699.2007.01724.x CrossRefGoogle Scholar
  53. Weis A, Melzer RR (2012a) How did sea spiders recolonize the Chilean fjords after glaciation? DNA barcoding of Pycnogonida, with remarks on phylogeography of Achelia assimilis (Haswell, 1885). Syst Biodivers 10:361–374. doi: 10.1080/14772000.2012.716462 CrossRefGoogle Scholar
  54. Weis A, Melzer RR (2012b) Chilean and Subantarctic Pycnogonida collected by the “Huinay Fjordos” Expeditions 2005–2011. Zool Reihe 88:185–203. doi: 10.1002/zoos.201200016 CrossRefGoogle Scholar
  55. Weis A, Meyer R, Dietz L et al (2014) Pallenopsis patagonica (Hoek, 1881)—a species complex revealed by morphology and DNA barcoding, with description of a new species of Pallenopsis Wilson, 1881. Zool J Linn Soc 170:110–131. doi: 10.1111/zoj.12097 CrossRefGoogle Scholar
  56. Wilcox TP, Hugg L, Zeh JA, Zeh DW (1997) Mitochondrial DNA sequencing reveals extreme genetic differentiation in a cryptic species complex of neotropical pseudoscorpions. Mol Phylogenet Evol 7:208–216CrossRefPubMedGoogle Scholar
  57. 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 152:895–904. doi: 10.1007/s00227-007-0742-9 CrossRefGoogle Scholar
  58. Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29:2869–2876. doi: 10.1093/bioinformatics/btt499/-/DC1 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Avril M. Harder
    • 1
  • Kenneth M. Halanych
    • 2
  • Andrew R. Mahon
    • 1
    Email author
  1. 1.Department of Biology, College of Science and TechnologyCentral Michigan UniversityMount PleasantUSA
  2. 2.Department of Biological Sciences and Molette Biology Laboratory for Environmental and Climate Change StudiesAuburn UniversityAuburnUSA

Personalised recommendations