Marine Biology

, Volume 151, Issue 5, pp 1839–1847

Genealogical relationships within and among shallow-water Ciona species (Ascidiacea)

Research Article

Abstract

In spite of historical and current interest in Ciona intestinalis and its congeners, little is known about evolutionary relationships among the members of the genus Ciona. Here 744-bp sequences of the mitochondrial cytochrome c oxidase subunit I (COI) gene are used to examine phylogenetic relationships among three described species (C. intestinalis, C. roulei, C. savignyi) sampled from multiple coastal sites in the Northeast Pacific (CA, USA), Northwest Atlantic (from New Hampshire to Connecticut, USA), Northeast Atlantic (Sweden and The Netherlands), and Mediterranean (Banyuls-sur-Mer, France). The samples were collected in June–October 2005. The COI sequences of Northeast Pacific/Mediterranean (Type A) and Northwest Atlantic (Type B) C. intestinalis differ by ∼12% and C. roulei is nested within Type B C. intestinalis. Ciona savignyi differs from all other haplotypes by 13–16%. A previously undescribed but morphologically distinct Ciona sp. found at the Banyuls-sur-Mer site was >10% divergent from all other haplotypes. Although these data arise from a single gene study, they indicate that further elucidation of species relationships within the genus and of the species’ distributions will be needed if continuing invasions and potential reproductive isolation are to be investigated.

References

  1. Arndt A, Marquez C, Lambert P, Smith MJ (1996) Molecular phylogeny of eastern Pacific sea cucumbers (Echinodermata: Holothuroidea) based on mitochondrial DNA sequence. Mol Phylogenet Evol 6:425–437PubMedCrossRefGoogle Scholar
  2. Biermann CH, Kessing BD, Palumbi SR (2003) Phylogeny and development of marine model species: strongylocentrotid sea urchins. Evol Dev 5:360–371PubMedCrossRefGoogle Scholar
  3. Boffelli D, Weer CV, Weng L, Lewis K, Shoukry MI, Pachter L, Keys DN, Rubin EM (2004) Intraspecies sequence comparisons for annotating genomes. Genome Res 14:2406–2411PubMedCrossRefGoogle Scholar
  4. Bucklin A, Guarnieri M, Hill RS, Bentley AM, Kaartvedt S (1999) Taxonomic and systematic assessment of planktonic copepods using mitochondrial COI sequence variation and competitive species-specific PCR. Hydrobiologia 401:239–254CrossRefGoogle Scholar
  5. Burton R (1995) Genetic differentiation and reproductive incompatibility among Baja California populations of the copepod Tigriopus californicus. Mar Biol 123:821–827CrossRefGoogle Scholar
  6. Byrd J, Lambert CC (2000) Mechanism of the block to hybridization and selfing between the sympatric ascidians Ciona intestinalis and Ciona savignyi. Mol Reprod Dev 55:109–116PubMedCrossRefGoogle Scholar
  7. Chabry L (1887) Contribution a l’embrologie normale teratologique des ascidies simples. J Anat Physiol Norm Path 23:167–319Google Scholar
  8. Copello M (1981) Ciona edwardsi (Roule, 1886) Espece littorale de Mediterranee distincte de Ciona intestinalis (Linne, 1767). Vie Milieu B Oceanog 31:243–253Google Scholar
  9. Dawson MN, Jacobs DK (2001) Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). Biol Bull 200:92–96PubMedCrossRefGoogle Scholar
  10. Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, Davidson B, Di Gregorio A et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167PubMedCrossRefGoogle Scholar
  11. Edmands S, Moberg PE, Burton RS (1996) Allozyme and mitochondrial DNA evidence of population subdivision in the purple sea urchin Strongylocentrotus purpuratus. Mar Biol 126:443–450CrossRefGoogle Scholar
  12. Fiala-Medioni A (1974) Ascidians of the rocky benthos of Banyuls-sur-Mer. Faunistic inventory and ecology notes. Vie Milieu B Oceanogr 24:193–207Google Scholar
  13. Gissi C, Pesole G (2003) Transcript mapping and genome annotation of ascidian mtDNA using EST Data. Genome Res 13:2203–2212PubMedCrossRefGoogle Scholar
  14. Glover AG, Goetze E, Dahlgren TG, Smith CR (2005) Morphology, reproductive biology and genetic structure of the whale-fall and hydrothermal vent specialist, Bathykurila guaymasensis Pettibone, 1989 (Annelida: Polynoidae). Mar Ecol P S Z N I 26:223–234CrossRefGoogle Scholar
  15. Harant H, Vernieres P (1933) Tuniciers. Faune de France 27:1–93Google Scholar
  16. Hart MW, Byrne M, Smith MJ (1997) Molecular phylogenetic analysis of life history evolution in Asterinid starfish. Evolution 51:1848–1861CrossRefGoogle Scholar
  17. Hellberg ME (1998) Sympatric sea shells along the sea’s shore: the geography of speciation in the marine gastropod Tegula. Evolution 52:1311–1324CrossRefGoogle Scholar
  18. Hill RS, Allen LD, Bucklin A (2001) Multiplexed species-specific PCR protocol to discriminate four N. Atlantic Calanus species, with an mtCOI gene tree for ten Calanus species. Mar Biol 139:279–287CrossRefGoogle Scholar
  19. 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 13:418–421PubMedGoogle Scholar
  20. Holland BS, Dawson MN, Crow GL, Hofmann DK (2004) Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands. Mar Biol 145:1119–1128CrossRefGoogle Scholar
  21. Hoshino ZI, Nishikawa T (1985) Taxonomic studies of Ciona intestinalis (L.) and its allies. Publ Seto Mar Biol Lab 30:61–79Google Scholar
  22. Hurtado LA, Lutz RA, Vrijenhoek RC (2004) Distinct patterns of genetic differentiation among annelids of eastern Pacific hydrothermal vents. Mol Ecol 13:2603–2615PubMedCrossRefGoogle Scholar
  23. Hurtado LA, Mateos M, Lutz RA, Vrijenhoek RC (2002) Molecular evidence for multiple species of Oasisia (Annelida: Siboglinidae) at eastern Pacific hydrothermal vents. Cah Biol Mar 34:377–380Google Scholar
  24. Jeffery WR, Swalla BJ (1990) Anural development in ascidians: evolutionary modification and elimination of the tadpole larva. Sem Dev Biol 1:253–261Google Scholar
  25. Johnson DS, Davidson B, Brown C, Smith W, Sidow A (2004) Noncoding regulatory sequences of Ciona exhibit strong correspondence between evolutionary constraint and functional importance. Genome Res 14:2448–2456PubMedCrossRefGoogle Scholar
  26. Jolly MT, Jollivet D, Gentil F, Thiebaut E, Viard F (2005) Sharp genetic break between Atlantic and English Channel populations of the polychaete Pectinaria koreni, along the North coast of France. Heredity 94:23–32PubMedCrossRefGoogle Scholar
  27. King TL, Eackles MS, Gjetvaj B, Hoeh WR (1999) Intraspecific phylogeography of Lasmigona subviridis (Bivalvia: Unionidae): conservation implications of range discontinuity. Mol Ecol 8:S65PubMedCrossRefGoogle Scholar
  28. Kott P (1952) The Ascidians of Australia. Aust J Mar Fresh Res 3:206–233CrossRefGoogle Scholar
  29. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  30. Lambert G (2001) A global overview of ascidian introductions and their possible impact on the endemic fauna. In: Sawada H, Yokosawa H, Lambert CC (eds) Proceedings of the first international symposium on the biology of ascidians. Springer, Tokyo, pp 249–257Google Scholar
  31. Lambert CC, Lambert G (2003) Persistence and differential distribution of nonindigenous ascidians in harbors of the Southern California Bight. Mar Ecol Prog Ser 259:145–161Google Scholar
  32. Lambert G, Lambert CC, Abbott D (1981) Corella species in the American Pacific Northwest: distinction of C. inflata Huntsman, 1912 from C. willmeriana Herdman 1898 (Ascidiacea, Phlebobranchiata). Can J Zool 59:1493–1504CrossRefGoogle Scholar
  33. Lambert CC, LaFargue F, Lambert G (1990) Preliminary note on the genetic isolation of Ciona species (Ascidiacea, Urochordata). Vie Milieu B Oceanogr 40:293–295Google Scholar
  34. Landry C, Geyer LB, Arakaki Y, Uehara Y, Palumbi SR (2003) Recent speciation in the Indo-West Pacific: rapid evolution of gamete recognition and sperm morphology in cryptic species of sea urchin. Proc R Soc Lond B 270:1839–1847CrossRefGoogle Scholar
  35. Lee CE (2000) Global phylogeography of a cryptic copepod species complex and reproductive isolation between genetically proximate ‘populations’. Evolution 54:2014–2027PubMedCrossRefGoogle Scholar
  36. Lessios HA, Kessing BD, Robertson DR, Paulay G (1999) Phylogeography of the pantropical sea urchin Eucidaris in relation to land barriers and ocean currents. Evolution 53:806–817CrossRefGoogle Scholar
  37. Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55:955–975PubMedCrossRefGoogle Scholar
  38. Linnaeus C (1767) Systema Naturae. Vindobonae: Typis Ioannis Thomae, pp 1767–1770Google Scholar
  39. McCartney MA, Keller G, Lessios GA (2000) Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Mol Ecol 9:1391–1400PubMedCrossRefGoogle Scholar
  40. Medina M, Weil E, Szmant AM (1999) Examination of the Montastraea annularis species complex (Cnidaria: Scleractinia) using ITS and COI sequences. Marine Biotechnol 1:89–97CrossRefGoogle Scholar
  41. Metz E (1998) Mitochondrial DNA and bindin gene sequence evolution among allopatric species of the sea urchin genus Arbacia. Mol Biol Evol 15:185–195PubMedGoogle Scholar
  42. Minganti A (1948) Interspecific fertilization in ascidians. Nature 161:643–644PubMedGoogle Scholar
  43. Missal K, Rose D, Stadler P (2005) Non-coding RNAs in Ciona intestinalis. Bioinformatics 21:i77–i78CrossRefGoogle Scholar
  44. Monniot C (1990) Ascidies de Nouvelle-Caledonie. 8. Phlebobranches (suite). B Mus Natl Hist Nat 12:491–515Google Scholar
  45. Monniot C, Monniot F (1977) Tuniciers benthiques profonds du Nord-Est Atlantique. Resultats des campagnes Biogas. B Mus Natl Hist Nat 323:695–720Google Scholar
  46. Monniot C, Monniot F (1983) Ascidies antarctiques et subantarctiques: morphologie et biogeographie. Mem Mus Natn Hist Nat Ser A 125:1–168Google Scholar
  47. Monniot C, Monniot F (1989) Ascidians collected around the Galapagos Islands using the Johnson Sea Link research submersible. P Biol Soc Wash 102:14–32Google Scholar
  48. Morgan TH (1904) Self-fertilization induced by artificial means. J Exp Zool 1:135–178CrossRefGoogle Scholar
  49. 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 131:497–503CrossRefGoogle Scholar
  50. Palumbi SR, Grabowsky G, Duda T, Geyer L, Tachino N (1997) Speciation and population genetic structure in tropical Pacific sea urchins. Evolution 51:1506–1517CrossRefGoogle Scholar
  51. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  52. Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175PubMedCrossRefGoogle Scholar
  53. Sanamyan K (1998) Ascidians from the north-western Pacific region. 5. Phlebobranchia. Ophelia 49:97–116Google Scholar
  54. Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis, ver 2.000. Genetics and Biometry Lab, Department of Anthropology, University of GenevaGoogle Scholar
  55. Sordino P, Heisenberg CP, Cirino P, Toscano A, Giuliano P, Marino R, Pinto MR, De-Santis R (2000) A mutational approach to the study of development of the protochordate Ciona intestinalis (Tunicata, Chordata). Sarsia 85:173–176Google Scholar
  56. Suzuki M, Nishikawa T, Bird A (2005) Genomic approaches reveal unexpected genetic divergence within Ciona intestinalis. J Mol Evol 61:627–635PubMedCrossRefGoogle Scholar
  57. Swofford DL (2003) PAUP*: phylogenetic analysis using parsimony and other methods), version 4.0b 10. Sinauer Associates, SunderlandGoogle Scholar
  58. Tarjuelo I, Posada D, Crandall KA, Pascual M, Turon X (2001) Cryptic species of Clavelina (Ascidiacea) in two different habitats: harbours and rocky littoral zones in the northwestern Mediterranean. Mar Biol 139:455–462CrossRefGoogle Scholar
  59. Tarjuelo I, Posada D, Crandall KA, Pascual M, Turon X (2004) Phylogeography and speciation of colour morphs in the colonial ascidian Pseudodistoma crucigaster. Mol Ecol 13:3125–3136PubMedCrossRefGoogle Scholar
  60. Van Name W (1945) The north and south American ascidians. B Am Mus Nat Hist 84:1–476Google Scholar
  61. van Syoc RJ (1994) Genetic divergence between subpopulations of the eastern Pacific goose barnacle Pollicipes elegans: mitochondrial cytochrome c subunit 1 nucleotide sequences. Mol Mar Biol Biotech 3:338–346Google Scholar
  62. Vinson J, Jaffe D, O’Neill K, Karlsson E, Stange-Thomann N, Anderson S, Mesirov J, Satoh N, Satou Y, Nusbaum C, Birren B, Galagan J, Lander E (2005) Assembly of polymorphic genomes: algorithms and application to Ciona savignyi. Genome Res 15:1127–1135PubMedCrossRefGoogle Scholar
  63. Yokobori S-i, Ueda T, Feldmaier-Fuchs G, Paeaebo S, Ueshima R, Kondow A, Nishikawa K, Watanabe K (1999) Complete DNA sequence of the mitochondrial genome of the ascidian Halocynthia roretzi (Chordata, Urochordata). Genetics 153:1851–1862Google Scholar
  64. Yokobori S-i, Watanabe Y, Oshima T (2003) Mitochondrial genome of Ciona savignyi (Urochordata, Ascidiacea, Enterogona): comparison of gene arrangement and tRNA genes with Halocynthia roretzi mitochondrial genome. J Mol Evol 57:574–587CrossRefGoogle Scholar
  65. Yokobori S-i, Oshima T, Wada H (2005) Complete nucleotide sequence of the mitochondrial genome of Doliolum nationalis with implications for evolution of urochordates. Mol Phylogenet Evol 34:273–283CrossRefGoogle Scholar
  66. Zigler KS, Raff EC, Popodi E, Raff RA, Lessios HA (2003) Adaptive evolution of bindin in the genus Heliocidaris is correlated with the shift to direct development. Evolution 57:2293–2302PubMedGoogle Scholar
  67. Zigler KS, Lessios HA (2004) Speciation on the coasts of the new world: phylogeography and the evolution of bindin in the sea urchin genus Lytechinus. Evolution 58:1225–1241PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyCornell UniversityIthacaUSA

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