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Marine Biology

, Volume 146, Issue 2, pp 213–222 | Cite as

Mitochondrial evolution and phylogeography in the hydrozoan Obelia geniculata (Cnidaria)

  • A. F. GovindarajanEmail author
  • K. M. Halanych
  • C. W. Cunningham
Research Article

Abstract

The distribution and genetic structure of many marine invertebrates in the North Atlantic have been influenced by the Pleistocene glaciation, which caused local extinctions followed by recolonization in warmer periods. Mitochondrial DNA markers are typically used to reconstruct species histories. Here, two mitochondrial markers [16S rDNA and cytochrome c oxidase I (COI)] were used to study the evolution of the widely distributed hydrozoan Obelia geniculata (Linnaeus, 1758) from the North Atlantic and the Pacific and, more specifically, in the context of North Atlantic phylogeography. Samples were collected from six geographic localities between 1998 and 2002. Hydroids from the North Atlantic, North Pacific (Japan), and South Pacific (New Zealand) are reciprocally monophyletic and may represent cryptic species. Using portions of the 16S rDNA and COI genes and the date of the last trans-Arctic interchange (3.1–4.1 million years ago), the first calibrated rate of nucleotide substitutions in hydrozoans is presented. Whereas extremely low substitution rates have been reported in other cnidarians, mainly based on anthozoans, substitution rates in O. geniculata are comparable to other invertebrates. Despite a life history that ostensibly permits substantial dispersal, there is apparently considerable genetic differentiation in O. geniculata. Divergence estimates and the presence of unique haplotypes provide evidence for glacial refugia in Iceland and New Brunswick, Canada. A population in Massachusetts, USA, appears to represent a relatively recent colonization event.

Keywords

Substitution Rate Glacial Maximum Glacial Refugium Ancestral Haplotype Substitution Rate Estimate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We are grateful to P. Schuchert, L.-A. Henry, Y. Hirano, and B. Grossman for providing specimens, and to F. Boero, L. Madin, J. Pineda, and T. Shank for helpful comments. This work was supported by an NSF PEET grant to C. Cunningham (DEB-9978131) and an Ocean Life Institute fellowship to K.M. Halanych. This is WHOI Contribution number 11181. The experiments comply with the current laws of the USA.

References

  1. Avise JC (2000) Phylogeography. Harvard University Press, CambridgeGoogle Scholar
  2. Berrill NJ (1948) A new method of reproduction in Obelia. Biol Bull (Woods Hole) 95:94–99Google Scholar
  3. Billard A (1904) Contribution a l’étude des hydroids (multiplication, regeneration, greffes, variations). Ann Sc Nat Zool 20:1–251Google Scholar
  4. Bodo F, Bouillon J (1968) Étude histologique du développement embryonnaire de quelques hydromédusas de Roscoff: Phialidium hemisphaericum (L.), Obelia sp. Péron et Lesueur, Sarsia exima (Allman), Podocoryne carnea (Sars), Gonionemus vertens Agassiz. Cah Biol Mar 9:69–104Google Scholar
  5. Boero F, Bouillon J (1993) Zoogeography and life cycle patterns of Mediterranean hydromedusae (Cnidaria). Biol J Linn Soc 48:239–266Google Scholar
  6. Bridge D, Cunningham CW, Schierwater B, DeSalle R, Buss LW (1992) Class-level relationships in the phylum Cnidaria: evidence from the mitochondrial genome structure. Proc Natl Acad Sci USA 89:8750–8753Google Scholar
  7. Bridge D, Cunningham CW, DeSalle R, Buss LW (1995) Class-level relationships in the phylum Cnidaria: molecular and morphological evidence. Mol Biol Evol 12:679–689Google Scholar
  8. Briggs JC (1970) A faunal history of the North Atlantic. Syst Zool 19:19–34Google Scholar
  9. Castelloe J, Templeton AR (1994) Root probabilities for intraspecific gene trees under neutral coalescent theory. Mol Phylogenet Evol 3:102–113Google Scholar
  10. Cornelius PFS (1975) The hydroid species of Obelia (Coelenterata, Hydrozoa, Campanulariidae), with notes on the medusa stage. Bull Br Mus Nat Hist (Zool Ser) 28:249–293Google Scholar
  11. Cornelius PFS (1990) European Obelia (Cnidaria, Hydrozoa): systematics and identification. J Nat Hist 24:535–578Google Scholar
  12. Cornelius PFS (1992) Medusa loss in leptolid Hydrozoa (Cnidaria), hydroid rafting, and abbreviated life-cycles among their remote-island faunae: an interim review. In: Bouillon J, Boero F, Cicogna F, Gili JM, Hughes RG (eds) Aspects of hydrozoan biology. Sci Mar 56:245–261Google Scholar
  13. Cornelius PFS (1995) North-west European thecate hydroids and their medusae, part 2. Sertulariidae to Campanulariidae. Synop Br Fauna New Ser 50:1–386Google Scholar
  14. Cunningham CW, Buss LW (1993) Molecular evidence for multiple episodes of paedomorphosis in the family Hydractiniidae. Biochem Syst Ecol 21:57–69Google Scholar
  15. Cunningham CW, Collins TM (1998) Beyond area relationships: extinction and recolonization in molecular marine biogeography. In: Schierwater B, Streit B, Wagner G, DeSalle R (eds) Molecular ecology and evolution: approaches and applications. Birkhauser, Basel, Switzerland, pp 297–321Google Scholar
  16. Cunningham CW, Buss LW, Anderson C (1991) Molecular and geologic evidence of shared history between hermit crabs and the symbiotic genus Hydractinia. Evolution 45:1301–1306Google Scholar
  17. Dahlgren TG, Weinberg JR, Halanych KM (2000) Phylogeography of the ocean quahog (Arctica islandica): influences of paleoclimate on genetic diversity and species range. Mar Biol 137:487–495Google Scholar
  18. Dawson AG (1992) Ice age earth: late quaternary geology and climate. Routledge, New YorkGoogle Scholar
  19. Dawson MN, Jacobs DK (2001) Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). Biol Bull (Woods Hole) 200:92–96Google Scholar
  20. Durham JW, MacNeil FS (1967) Cenozoic migrations of marine invertebrates through the Bering Strait region. In: Hopkins DM (ed) The Bering land bridge. Stanford University Press, Stanford, Calif., USA, pp 326–349Google Scholar
  21. Edwards SV, Beerli P (2000) Perspective: gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evolution 54:1839–1854Google Scholar
  22. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299Google Scholar
  23. France SC, Hoover LL (2001) Analysis of variation in mitochondrial DNA sequences (ND3, ND4L, MSH) among Octocorallia (=Alcyonaria) (Cnidaria: Anthozoa). Bull Biol Soc Wash 10:110–118Google Scholar
  24. France SC, Hoover LL (2002) DNA sequences of the mitochondrial COI gene have low levels of divergence among deep-sea octocorals (Cnidaria: Anthozoa). Hydrobiologia 471:149–155Google Scholar
  25. Franz DR, Merrill AS (1980a) Molluscan distribution patterns on the continental shelf of the Middle Atlantic Bight (Northwest Atlantic). Malacologia 19:209–225Google Scholar
  26. Franz DR, Merrill AS (1980b) The origins and determinants of distribution of molluscan faunal groups on the shallow continental shelf of the northwest Atlantic. Malacologia 19:227–248Google Scholar
  27. Gladenkov AY, Oleinik AE, Marincovich Jr L, Barinov KB (2002) A refined age for the earliest opening of the Bering Strait. Palaeogeogr Palaeoclimatol Palaeoecol 183:321–328Google Scholar
  28. Hamner WM, Hamner PP, Strand SW (1994) Sun-compass migration by Aurelia aurita (Scyphozoa): population retention and reproduction in Saanich Inlet, British Columbia. Mar Biol 119:347–356Google Scholar
  29. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913Google Scholar
  30. Hoeh WR, Stewart DT, Sutherland BW, Zouros E (1996) Cytochrome c oxidase sequence comparisons suggest an unusually high rate of mitochondrial DNA evolution in Mytilus (Mollusca: Bivalvia). Mol Biol Evol 13:418–421Google Scholar
  31. Holder K, Montgomerie R, Friesen VL (1999) A test of the glacial refugium hypothesis using patterns of mitochondrial and nuclear DNA sequence variation in rock ptarmigan (Lagopus mutus). Evolution 53:1936–1950Google Scholar
  32. Huelsenbeck JP, Rannala B (1997) Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science 276:227–232Google Scholar
  33. Ingolfsson A (1992) The origin of the rocky shore fauna of Iceland and the Canadian Maritimes. J Biogeogr 19:705–712Google Scholar
  34. Ingolfsson A (1995) Floating clumps of seaweed around Iceland: natural microcosms and a means of dispersal for shore fauna. Mar Biol 122:13–21Google Scholar
  35. Knowlton N, Weigt LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proc R Soc Lond B Biol Sci 265:2257–2263Google Scholar
  36. Kramp PL (1927) The hydromedusae of Danish waters. K Dan Vidensk Selsk Biol Skr 8:1–291Google Scholar
  37. Maddison WP, Maddison DR (2000) MacClade: analysis of phylogeny and character evolution, ver. 4.0. Sinauer, Sunderland, Mass., USAGoogle Scholar
  38. Marincovich Jr L, Gladenkov AY (1999) Evidence for an early opening of the Bering Strait. Nature 397:149–151Google Scholar
  39. Marincovich Jr L, Gladenkov AY (2001) New evidence for the age of the Bering Strait. Quat Sci Rev 20:329–335Google Scholar
  40. Medina M, Weil E, Szmant AM (1999) Examination of the Montastraea annularis species complex (Cnidaria: Scleractinia) using ITS and COI sequences. Mar Biotechnol 1:89–97Google Scholar
  41. Palumbi SR, Kessing BD (1991) Population biology of the trans-Arctic exchange: mtDNA sequence similarity between Pacific and Atlantic sea urchins. Evolution 45:1790–1805Google Scholar
  42. Panteleeva NN (1999) Obelia longissima (Pallas, 1766) and Obelia geniculata (L., 1758) (Hydrozoa, Thecaphora, Campanulariidae) in the Barents Sea. Morphology, distribution, ecology and special life history features. Zoosyst Rossica Suppl 1:51–65Google Scholar
  43. Pielou EC (1991) After the ice age. University of Chicago Press, ChicagoGoogle Scholar
  44. Pont-Kingdon GA, Okada NA, Macfarlane JL, Beagley CT, Wolstenholme DR, Cavalier-Smith T, Clark-Walker GD (1995) A coral mitochondrial MutS gene. Nature 375:109–111Google Scholar
  45. Pont-Kingdon G, Okada NA, Macfarlane JL, Beagley CT, Watkins-Sims CD, Cavalier-Smith T, Clark-Walker GD, Wolstenholme DR (1998) Mitochondrial DNA of the coral Sarcophyton glaucum contains a gene for a homologue of bacterial MutS: a possible case of gene transfer from the nucleus to the mitochondrion. J Mol Evol 46:419–431Google Scholar
  46. Posada D, Crandall KA (1998) ModelTest: testing the model of DNA substitution. Bioinformatics 14:817–818Google Scholar
  47. Ralph PM (1956) Variation in Obelia geniculata (Linnaeus, 1758) and Silicularia bilabiata (Coughtrey, 1875) (Hydroida, f. Campanulariidae). Trans R Soc NZ 84:279–296Google Scholar
  48. Rogerson RJ (1983) Geological evolution. In: South RG (ed) Biogeography and ecology of the island of Newfoundland. Junk, The Hague, The NetherlandsGoogle Scholar
  49. Romano SL, Palumbi SR (1997) Molecular evolution of a portion of the mitochondrial 16S ribosomal gene region in scleractinian corals. J Mol Evol 45:397–411Google Scholar
  50. Saillard J, Forster P, Lynnerup N, Bandelt H, Norby S (2000) MtDNA variation among Greenland eskimos: the edge of the Beringian expansion. Am J Hum Genet 67:718–726Google Scholar
  51. Schneider S, Roessli D, Excoffier L (2000) Arlequin, ver. 2.000. A software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  52. Schubart CD, Diesel R, Hedges SB (1998) Rapid evolution to terrestrial life in Jamaican crabs. Nature 393:363–365Google Scholar
  53. Shearer TL, Van Oppen MJH, Romano SL, Worheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487Google Scholar
  54. Siegert MJ (2001) Ice sheets and Late Quaternary environmental change. Wiley, Chichester, EnglandGoogle Scholar
  55. Snell TL, Foltz DW, Sammarco PW (1998) Variation in morphology vs conservation of a mitochondrial gene in Montastraea cavernosa (Cnidaria, Scleractinia). Gulf Mexico Sci 16:188–195Google Scholar
  56. Sommer C (1992) Larval biology and dispersal of Eudendrium racemosum (Hydrozoa, Eudendriidae). In: Bouillon J, Boero F, Cicogna F, Gili JM, Hughes RG (eds) Aspects of hydrozoan biology. Sci Mar 56:205–211Google Scholar
  57. Stam WT, Bot PVM, Boele-Bos SA, van Rooij JM, van den Hoek C (1988) Single-copy DNA–DNA hybridizations among five species of Laminaria (Phaeophyceae): phylogenetic and biogeographic implications. Helgol Meeresunters 42:251–267Google Scholar
  58. Swofford DL (2000) PAUP* (phylogenetic analysis using parsimony). Sinauer, Sunderland, Mass., USAGoogle Scholar
  59. 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 22:4673–4680Google Scholar
  60. Torroni A, Bandelt H, D’Urbano L, Lahermo P, Moral P, Sellitto D, Rengo C, Forster P, Savontaus M, Bonne-Tamir B, Scozzari R (1998) MtDNA analysis reveals a major late Paleolithic population expansion from southwestern to northeastern Europe. Am J Hum Genet 62:1137–1152Google Scholar
  61. Van den Hoek C, Breeman AM (1990) Seaweed biogeography of the North Atlantic: where are we now? In: Garbary DJ, South GR (eds) Evolutionary biogeography of marine algae in the North Atlantic. NATO ASI Ser G22, Springer, New York Berlin Heidelberg, pp 55–87Google Scholar
  62. Van Oppen MJH, Draisma SGA, Olsen JL, Stam WT (1995) Multiple trans-Arctic passages in the red alga Phycodrys rubens: evidence from nuclear rDNA ITS sequences. Mar Biol 123:179–188Google Scholar
  63. Van Oppen MJH, Willis BL, Miller DJ (1999) Atypically low rate of cytochrome b evolution in the scleractinian coral genus Acropora. Proc R Soc Lond B Biol Sci 266:179–183Google Scholar
  64. Vermeij G (1991) Anatomy of an invasion: the trans-Arctic interchange. Paleobiology 17:281–307Google Scholar
  65. Wares JP (2001) Patterns of speciation inferred from mitochondrial DNA in North American Chthamalus (Cirripedia: Balanomorpha: Chthamaloidea). Mol Phylogenet Evol 18:104–116Google Scholar
  66. Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55:2455–2469Google Scholar
  67. Wares JP, Goldwater DS, Kong BY, Cunningham CW (2002) Refuting a controversial case of human-mediated marine species introduction. Ecol Lett 5:577–584Google Scholar
  68. Young AMC, Torres JE, Mack JE, Cunningham CW (2002) Morphological and genetic evidence for vicariance and refugium in the Atlantic and Gulf of Mexico populations of the hermit crab Pagurus longicarpus. Mar Biol 140:1059–1066Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • A. F. Govindarajan
    • 1
    Email author
  • K. M. Halanych
    • 1
    • 3
  • C. W. Cunningham
    • 2
  1. 1.Biology DepartmentWoods Hole Oceanographic InstitutionWoods HoleUSA
  2. 2.Biology DepartmentDuke UniversityDurhamUSA
  3. 3.Biological Sciences Dept.Auburn UniversityAuburnUSA

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