Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands

Abstract

The upside-down jellyfish Cassiopea is a globally distributed, semi-sessile, planktonically dispersed scyphomedusa. Cassiopea occurs in shallow, tropical inshore marine waters on sandy mudflats and is generally associated with mangrove-dominated habitats. Controversy over the taxonomy of upside-down jellyfishes precedes their introduction to the Hawaiian Islands during the Second World War, and persists today. Here we address the global phylogeography and molecular systematics of the three currently recognized species: Cassiopea andromeda, C. frondosa, and C. xamachana. Mitochondrial cytochrome c oxidase I (COI) sequences from Australia, Bermuda, Fiji, the Florida Keys, the Hawaiian Islands, Indonesia, Palau, Panama, Papua New Guinea, and the Red Sea were analyzed. Highly divergent COI haplotypes within the putative species C. andromeda (23.4% Kimura 2-parameter molecular divergence), and shared haplotypes among populations of two separate putative species, C. andromeda and C. xamachana from different ocean basins, suggest multiple anthropogenic introductions and systematic confusion. Two deeply divergent O’ahu haplotypes (20.3%) from morphologically similar, geographically separate invasive populations indicate long-term (14–40 million years ago) reproductive isolation of phylogenetically distinct source populations and cryptic species. Data support at least two independent introductions to the Hawaiian Islands, one from the Indo-Pacific, another from the western Atlantic/Red Sea. Molecular phylogenetic results support six species: (1) C. frondosa, western Atlantic (2) C. andromeda, Red Sea/western Atlantic/Hawaiian Islands (3) C. ornata, Indonesia/Palau/Fiji (4) Cassiopea sp. 1, eastern Australia (5) Cassiopea sp. 2, Papua New Guinea and (6) Cassiopea sp. 3, Papua New Guinea/Hawaiian Islands.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Agassiz A, Mayer AG (1899) Acalephs from the Fiji Islands. Bull Mus Comp Zool 32:157–189

    Google Scholar 

  2. Arai MN (2001) Pelagic coelenterates and eutrophication: a review. Hydrobiologia 451:68–87

    Article  Google Scholar 

  3. Baldwin B, Robichaux RH (1995) Historical biogeography and ecology of the Hawaiian silversword alliance (Asteraceae): new molecular phylogenetic perspectives. In: Wagner WL, Funk VA (eds) Hawaiian biogeography: evolution on a hot spot archipelago. Smithsonian Institution Press, Washington, pp 259–287

  4. Bowers N, Stauffer JR, Kocher TD (1994) Intra- and interspecific mitochondrial DNA sequence variation within two species of rock-dwelling cichlids (Teleostei: Cichlidae) from Lake Malawi, Africa. Mol Phylogenet Evol 3:75–82

    Article  CAS  PubMed  Google Scholar 

  5. Buckley TR, Simon C, Chambers GK (2001) Phylogeography of the New Zealand cicada Maoricicada campbelli based on mitochondrial DNA sequences: ancient clades associated with Cenozoic environmental change. Evolution 55:1395–1407

    CAS  PubMed  Google Scholar 

  6. Bucklin A, Bentley AM, Franzen SP (1998) Distribution and relative abundance of the copepods, Pseudocalanus moultoni and P. newmani, on Georges Bank based on molecular identification of sibling species. Mar Biol 132:97–106

    Article  CAS  Google Scholar 

  7. Caccone A, Sbordoni V (2001) Molecular biogeography of cave life: a study using mitochondrial DNA from bathysciine beetles. Evolution 55:122–130

    CAS  PubMed  Google Scholar 

  8. Carlton JT (1989) Man’s role in changing the face of the ocean: biological invasions and implications for conservation of nearshore environments. Conserv Biol 265–273

  9. Carranza S, Arnold EN, Mateo JA, Geniez P (2002) Relationships and evolution of the North African geckos, Geckonia and Tarentola (Reptilia: Gekkonidae), based on mitochondrial and nuclear DNA sequences. Mol Phylogenet Evol 23:244–256

    Article  CAS  PubMed  Google Scholar 

  10. Castilla JC, Collins AG, Meyer CP, Guiñez R, Lindberg DR (2002) Recent introduction of the dominant tunicate, Pyura praenuptialis (Urochordata, Pyuridae) to Antofagasta, Chile. Mol Ecol 11:1579–1584

    Article  CAS  PubMed  Google Scholar 

  11. Collin R (2000) Phylogeny of the Crepidula plana (Gastropoda: Calyptraeidea) cryptic species complex in North America. Can J Zool 78:1500–1514

    Article  Google Scholar 

  12. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    Article  PubMed  Google Scholar 

  13. Cywinska A, Hebert PDN (2002) Origins and clonal diversity in the hypervariable asexual ostracod Cypridopsis vidua. J Evol Biol 15:134–145

    Article  Google Scholar 

  14. Dawson MN (2003) Macro-morphological variation among cryptic species of the moon jellyfish, Aurelia (Cnidaria: Scyphozoa). Mar Biol 143:369–379. Erratum. Mar Biol 144:203

    Article  Google Scholar 

  15. Dawson MN, Jacobs DK (2001) Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). Biol Bull 200:92–96

    CAS  PubMed  Google Scholar 

  16. Doty MS (1961) Acanthophora, a possible invader of the marine flora of Hawai’i. Pac Sci 15:547–552

    Google Scholar 

  17. Eldredge LG, Carlton JT (2002) Hawaiian marine bioinvasions: a preliminary report. Pac Sci 56:211–212

    Google Scholar 

  18. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  19. Fleck J, Fitt WK (1999) Degrading leaves of Rhizophora mangle Linné provide a natural cue for settlement and metamorphosis of the upside down jellyfish Cassiopea xamachana. J Exp Mar Biol Ecol 234:83–94

    Article  Google Scholar 

  20. Flowers JM, Schroeter SC, Burton RS (2002) The recruitment sweepstakes has many winners: genetic evidence from purple sea urchins. Evolution 56:1445–1453

    CAS  PubMed  Google Scholar 

  21. 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 Biotech 3:294–299

    CAS  Google Scholar 

  22. Funk DJ (1999) Molecular systematics of cytochrome oxidase I and 16S from Neochlamisus leaf beetles and the importance of sampling. Mol Biol Evol 16:67–82

    CAS  PubMed  Google Scholar 

  23. Gohar HAF, Eisawy AM (1960) The biology of Cassiopea andromeda (from the Red Sea) (With a note on the species problem). Publ Mar Biol Stat Ghardaqa 11:3–39

    Google Scholar 

  24. Gómez A, Snell TW (1996) Sibling species in the Brachionus plicatilis species complex. J Evol Biol 9:953–964

    Google Scholar 

  25. Gómez A, Serra M, Carvalho GR, Lunt DH (2002) Speciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus plicatilis. Evolution 56:1431–1444

    PubMed  Google Scholar 

  26. Haeckel EHPA (1880) Das system der medusen: erster theil einer monographie der medusen. Fischer, Jena

    Google Scholar 

  27. Hart MW, Byrne M, Smith MJ (1997) Molecular phylogenetic analysis of life-history evolution in asterinid starfish. Evolution 51:1846–1859

    Google Scholar 

  28. Hebert PDN, Cywinska A, Ball SL, de Waard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–322

    Article  CAS  PubMed  Google Scholar 

  29. Herke SW, Foltz DW (2002) Phylogeography of two squid (Loligo pealei and L. plei) in the Gulf of Mexico and northwestern Atlantic Ocean. Mar Biol 140:103–115

    Article  CAS  Google Scholar 

  30. Hofmann DK, Hadfield MG (2002) Hermaphroditism, gonochorism, and asexual reproduction in Cassiopea sp.—an immigrant in the islands of Hawai‘i. Invertebr Reprod Dev 41:215–221

    Google Scholar 

  31. Holland BS (2000) Genetics of marine bioinvasions. Hydrobiologia 420:63–71

    Article  CAS  Google Scholar 

  32. Holland BS, Hadfield MG (2002) Islands within an island: phylogeography and conservation genetics of the endangered Hawaiian tree snail Achatinella mustelina. Mol Ecol 11:365–376

    Article  CAS  PubMed  Google Scholar 

  33. Hummelinck PW (1968) Caribbean scyphomedusae of the genus Cassiopea. studies of fauna of Curaçao and other Caribbean Islands 23:1131–1143

  34. Jordal BH, Normark BB, Farell BD, Kirkendall LR (2002) Extraordinary haplotype diversity in haplodiploid inbreeders: phylogenetics and evolution of the bark beetle genus Coccotrypes. Mol Phylogenet Evol 23:171–188

    Article  CAS  PubMed  Google Scholar 

  35. Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420:73–90

    Article  CAS  Google Scholar 

  36. Knowlton N, Weigt LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proc R Soc Lond B 265:2257–2263

    Article  Google Scholar 

  37. Kramp PL (1970) Zoogeographical studies on Rhizostomae (Scyphozoa). Vidensk Medd Dan Naturhist Foren Khobenhavn 133:7–30

    Google Scholar 

  38. Lessios HA (1998) The first stage of speciation as seen in organisms separated by the Isthmus of Panama. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, New York, pp 186–201

  39. Mallet J (2001) The speciation revolution. J Evol Biol 14:887–888

    Article  Google Scholar 

  40. Mayer AG (1906) Medusae of the Hawaiian Islands collected by the steamer Albatross in 1902. Bull US Fish Comm 23:1131–1143

    Google Scholar 

  41. Mayr E, Ashlock PD (1993) Principles of systematic zoology, 2nd edn. McGraw-Hill, New York, N.Y.

  42. Meyer A, Knowles LL, Verheyen E (1996) Widespread geographical distribution of mitochondrial haplotypes in rock-dwelling cichlid fishes from Lake Tanganyika. Mol Ecol 5:341–350

    Article  CAS  PubMed  Google Scholar 

  43. Meyran JC, Monnerot M, Taberlet P (1997) Taxonomic status and phylogenetic relationships of some species of the genus Gammarus (Crustacea, Amphipoda) deduced from mitochondrial DNA sequences. Mol Phylogenet Evol 8:1–10

    Article  CAS  PubMed  Google Scholar 

  44. Mills CE (2001) Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Hydrobiologia 451:55–68

    Article  Google Scholar 

  45. O’Foighil D, Gaffney PM, Wilbur AE, Hilbish TJ (1998) Mitochondrial cytochrome oxidase I gene sequences support an Asian origin for the Portuguese oyster Crassostrea angulata. Mar Biol 131:497–503

    Article  Google Scholar 

  46. Palumbi SR (1997) Molecular biogeography of the Pacific. Coral Reefs 16:47–52

    Article  Google Scholar 

  47. Peek AS, Gaut BS, Feldman RA, Barry JP, Kochevar RE, Lutz RA, Vrijenhoek RC (2000) Neutral and nonneutral mitochondrial genetic variation in deep-sea clams from the family Vesicomyidae. J Mol Evol 50:141–153

    CAS  PubMed  Google Scholar 

  48. Rundell RJ, Holland BS, Cowie RC (2004) Molecular Phylogeography of the endemic Hawaiian Succineidae (Gastropoda: Pulmonata). Mol Phylogenet Evol 31:246–255

    Article  CAS  PubMed  Google Scholar 

  49. Sax DF (2001) Latitudinal gradients and geographic ranges of exotic species: implications for biogeography. J Biogeogr 28:139–150

    Article  Google Scholar 

  50. Tarr CL, Fleischer RC (1995) Evolutionary relationships of the Hawaiian honeycreepers (Aves: Drepanidae). In: Wagner WL, Funk VA (eds) Hawaiian biogeography: evolution on a hot spot archipelago. Smithsonian Institution Press, Washington, pp 147–159

  51. Tautz D, Arctander P, Minelli A, Thomas RH, Vogler AP (2003) A plea for DNA taxonomy. Trends Ecol Evol 18:70–74

    Article  Google Scholar 

  52. Templeton AR (1989) The meaning of species and speciation: a genetic perspective. In: Otte D, Endler JA (eds) Speciation and its consequences. Sinauer, Sunderland, Mass., pp 3–27

  53. Thiel VME (1975) Bemerkungen zur Systematik der Gattung Cassiopea (Cepheida, Scyphomedusae). Mitt Hamb Zool Mus Inst 72:25–46

    Google Scholar 

  54. Trewick SA, Wallis GP, Morgan-Richards M (2000) Phylogeographical pattern correlates with Pliocene mountain building in the alpine scree weta (Orthoptera, Anostostomatidae). Mol Ecol 9:657–666

    Article  CAS  PubMed  Google Scholar 

  55. Uchida T (1970) Occurrence of a rhizostome medusa, Cassiopea mertensii Brandt from the Hawaiian Islands. Annot Zool Jpn 43:102–104

    Google Scholar 

  56. Williams ST (2000) Species boundaries in the starfish genus Linckia. Mar Biol 136:137–148

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Professor Mike Hadfield for providing support and research facilities at the Kewalo Marine Laboratory, University of Hawai’i, and to Professor John Benzie for facilities at the Centre for Marine and Coastal Studies, University of New South Wales (UNSW). We thank William Puleloa, Tom Iwai, Lori Colin, Bert Hoeksema, Harilaos Lessios, Don de Maria, Laura Martin, David Miller, Kylie Pitt, Alan Nelson, Kirk Murakami, and Dan Lindstrom for providing medusae specimens. Thanks to Kualoa Ranch and Mid-Pacific Golf Course for providing access. François Seneca assisted in laboratory DNA extractions. Thanks to Dr. Jonathan Gardner, Victoria University, New Zealand for valuable comments on an earlier draft of this manuscript. We also thank Aquarium Solutions International, Ruhr-Universität Bochum, and the Vice-Chancellor’s Post-doctoral Fellowship scheme (UNSW) for financial support. The experiments performed during the course of this study are in full compliance with the current laws of the United States.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Brenden S. Holland.

Additional information

Communicated by P.W. Sammarco, Chauvin

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Holland, B.S., Dawson, M.N., Crow, G.L. et al. Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands. Marine Biology 145, 1119–1128 (2004). https://doi.org/10.1007/s00227-004-1409-4

Download citation

Keywords

  • Reproductive Isolation
  • Cryptic Species
  • Hawaiian Island
  • Pairwise Sequence Divergence
  • Moon Jellyfish