Marine Biology

, Volume 159, Issue 7, pp 1611–1619 | Cite as

Field identification of ‘types’ A and B of the ascidian Ciona intestinalis in a region of sympatry

  • Atsuko SatoEmail author
  • Nori Satoh
  • John D. D. Bishop


The ascidian species Ciona intestinalis is a major model chordate in developmental and evolutionary biology, and an important fouling organism and invasive species. However, genomic investigation has recently revealed the existence of two cryptic species, genetically distinct yet without obvious morphological differences, currently referred to as types A and B. Here, we show that they are externally distinctive in a zone of sympatry in the western English Channel. Examining genotyped specimens, we found that types A and B of C. intestinalis can generally be distinguished by body colour, pigmentation at the distal end of the siphons and the presence or absence of tubercles on the sides of the siphons. Detecting specimens of hybrid descent still requires detailed molecular analysis, but these visual characters in combination will identify living specimens of types A and B with high probability. These differences are shown to be inherited.


Cryptic Species Natural Hybrid Body Colour Hybrid Cross Orange Pigment 
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.



We thank Chris Wood, Linda Noble, Colin Brownlee and other staff of the Marine Biological Association of the UK for generous hospitality during work on C. intestinalis. We also thank Seb Shimeld for valuable comments and laboratory space and resources for genotyping, Marie Nydam for advice on genotyping, Andy Griffiths for advice in genome extraction, and Takeshi Kawashima, Takeshi Nakashima and Mayuko Hamada for helpful discussion. This research was funded by a Ray Lankester Investigatorship from the Marine Biological Association of the UK, the AXA Research Fund, the Okinawa Institute of Science and Technology, and a JSPS Fellowship for Study Abroad to A.S.

Supplementary material

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  1. Ärnbäck-Christie-Linde A (1923) A list of ascidians collected off Gothenburg. Meddn Göteborgs Mus Zool Ardeln 28:1–19Google Scholar
  2. Auger H, Sasakura Y, Joly J-S, Jeffery WR (2010) Regeneration of oral siphon pigment organs in the ascidian Ciona intestinalis. Dev Biol 339:374–389CrossRefGoogle Scholar
  3. Berrill NJ (1950) The Tunicata with an account of the British species. Ray Society, LondonGoogle Scholar
  4. Bickford D, Lohman DJ, Sodhi NS, Ng PK, Meier R, Winker K, Ingram KK, Das I (2006) Cryptic species as a window on diversity and conservation. Trend Ecol Evol 22:148–155CrossRefGoogle Scholar
  5. Boffelli D, Weer CV, Weng L, Lewis KD, Shoukry MI, Pachter L, Keys DN, Rubin EM (2004) Intraspecies sequence comparisons for annotating genomes. Genome Res 14:2406–2411CrossRefGoogle Scholar
  6. Caputi L, Andreakis N, Mastrototaro F, Cirino P, Vassillo M, Sordino P (2007) Cryptic speciation in a model invertebrate chordate. PNAS 104:9364–9369CrossRefGoogle Scholar
  7. Caputi L, Borra M, Andreakis N, Biffali E, Sordino P (2008) SNPs and Hox gene mapping in Ciona intestinalis. BMC Genomics 9:39CrossRefGoogle Scholar
  8. Daigle R, Herbinger C (2009) Ecological interactions between the vase tunicate (Ciona intestinalis) and the farmed blue mussel (Mytilus edulis) in Nova Scotia, Canada. Aquat Invasions 4:177–187CrossRefGoogle Scholar
  9. Dehal P, Satou Y, Campbell RK et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2166CrossRefGoogle Scholar
  10. Dybern BI (1965) The life cycle of Ciona intestinalis (L.) f. typica in relation to the environmental temperature. Oikos 16:109–131CrossRefGoogle Scholar
  11. Hoshino ZI, Nishikawa T (1985) Taxonomic studies of Ciona intestinalis (L.) and its allies. Publ Seto Mar Biol Lab 30:61–79Google Scholar
  12. Iannelli F, Pesole G, Sordino P, Gissi C (2007) Mitogenomics reveals two cryptic species in Ciona intestinalis. Trends Genet 23:419–421CrossRefGoogle Scholar
  13. Jeffery WR, Chiba T, Krajka FR, Deyts D, Satoh N, Joly JS (2008) Trunk lateral cells are neural crest-like cells in the ascidian Ciona intestinalis: insights into the ancestry and evolution of the neural crest. Dev Biol 324:152–160CrossRefGoogle Scholar
  14. Kano S (2007) Initial stage of genetic mapping in Ciona intestinalis. Dev Dyn 236:1768–1781CrossRefGoogle Scholar
  15. Kano S, Chiba S, Satoh N (2001) Genetic relatedness and variability in inbred and wild populations of the solitary ascidian Ciona intestinalis revealed by arbitrarily primed polymerase chain reaction. Mar Biotechnol (NY) 3:58–67CrossRefGoogle Scholar
  16. Millar RH (1953) Ciona. L.M.B.C. Memoirs on typical British marine plants and animals, 35, i-iv and 1-123. Liverpool University Press, LiverpoolGoogle Scholar
  17. Nydam ML, Harrison RG (2007) Genealogical relationships within and among shallow-water Ciona species (Ascidiacea). Mar Biol 151:1839–1847CrossRefGoogle Scholar
  18. Nydam ML, Harrison RG (2010) Polymorphism and divergence within the ascidian genus Ciona. Mol Phyl Evol 56:718–726CrossRefGoogle Scholar
  19. Nydam ML, Harrison RG (2011a) Introgression despite substantial divergence in a broadcast spawning marine invertebrate. Evolution 65:429–442CrossRefGoogle Scholar
  20. Nydam ML, Harrison RG (2011b) Reproductive protein evolution in two cryptic species of marine chordate. BMC Evol Biol 11:18CrossRefGoogle Scholar
  21. Putnam NH, Butts T, Ferrier DE, Furlong RF, Fellsten U et al (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064–1071CrossRefGoogle Scholar
  22. Ramsay A, Davidson J, Bourque D, Stryhn H (2009) Recruitment patterns and population development of the invasive ascidian Ciona intestinalis in Prince Edward Island, Canada. Aquat Invasions 4:169–176CrossRefGoogle Scholar
  23. Satoh N (1994) Developmental biology of ascidians. Cambridge University Press, CambridgeGoogle Scholar
  24. Satoh N (2003) The ascidian tadpole larva: comparative molecular development and genomics. Nat Rev Genet 4:285–295CrossRefGoogle Scholar
  25. Shenkar N, Swalla BJ (2011) Global diversity of Ascidiacea. PLoS One 6:e20657CrossRefGoogle Scholar
  26. Suzuki MM, Nishikawa T, Bird A (2005) Genomic approaches reveal unexpected genetic divergence within Ciona intestinalis. J Mol Evol 61:627–635CrossRefGoogle Scholar
  27. Van Name WG (1945) The North and South American ascidians. Bull Am Mus Nat Hist 84:1–476 (pp 162–163 about longissima)Google Scholar
  28. Zeller RW (2010) Int Comp Biol 50:cover pageGoogle Scholar
  29. Zhan A, Macisaac HJ, Cristescu ME (2010) Invasion genetics of the Ciona intestinalis species complex: from regional endemism to global homogeneity. Mol Ecol 19:4678–4694CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Atsuko Sato
    • 1
    • 2
    • 3
    Email author
  • Nori Satoh
    • 2
  • John D. D. Bishop
    • 3
  1. 1.Department of ZoologyUniversity of OxfordOxfordUK
  2. 2.Marine Genomics Unit, Okinawa Institute of Science and TechnologyKunigamiJapan
  3. 3.The LaboratoryMarine Biological Association of the UKPlymouthUK

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