Skip to main content
Log in

High natural fusion rates in a botryllid ascidian

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Many benthic colonial invertebrates have the ability to fuse and form chimeras with compatible colonies. Botryllid ascidians are model organisms for the study of the evolution of and molecular basis for allorecognition, and fusion rates have been determined for different populations and species by random sampling and fusion testing between individuals. However, natural fusion rates over time have not been documented. Nine settlement panels were deployed in Salem Harbor, Massachusetts, USA and Botrylloides violaceus settlement, growth, and fusion monitored from July to mid-August 2007. Seventy-three percent of the recruits observed fused with at least one other colony, while 4% neither fused nor were overgrown. Multifused colonies were not observed to grow faster than single colonies when growth was calculated as increase in size beyond the summation of fused entities; however, they were significantly larger. These results suggest that larvae settle in clumps of compatible individuals, and that large subtidal colonies may be the result of high numbers of fusions between compatible colonies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Ben-Shlomo R, Motro U, Paz G, Rinkevich B (2008) Pattern of settlement and natural chimerism in the colonial urochordate Botryllus schlosseri. Genetica 132:51–58

    Article  Google Scholar 

  • Bishop JDD, Sommerfeldt AD (1999) Not like Botryllus: indiscriminate post-metamorphic fusion in a compound ascidian. Proc R Soc Lond B Biol Sci 266:241–248

    Article  Google Scholar 

  • Burnet FM (1971) “Self-recognition” in colonial marine forms and flowering plants in relation to the evolution of immunity. Nature 232:230–235

    Article  CAS  Google Scholar 

  • Buss LW (1982) Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc Nat Acad of Sci U S A 79:5337–5341

    Article  CAS  Google Scholar 

  • Chadwick-Furman NE, Weissman IL (1995) Life history plasticity in chimaeras of the colonial ascidian Botryllus schosseri. Proc R Soc Lond B Biol Sci 262:157–162

    Article  CAS  Google Scholar 

  • Chadwick-Furman NE, Weissman IL (2003) Effects of allogeneic contact on life-history traits of the colonial ascidian Botryllus schlosseri in Monterey Bay. Biol Bull (Woods Hole) 205:133–143

    Article  Google Scholar 

  • De Tomaso AW (2006) Allorecognition polymorphism versus parasitic stem cells. Trends Genet 22:485–490

    Article  CAS  Google Scholar 

  • Dijkstra J, Harris L, Westerman E (2007) Distribution and long-term temporal patterns of four invasive colonial ascidians in the Gulf of Maine. J Exp Mar Biol Ecol 342:61–68

    Article  Google Scholar 

  • Grey EK (2009) Do we need to jump in? A comparison of two survey methods of exotic ascidians on docks. Aquat Invasions 4:81–86

    Article  Google Scholar 

  • Grosberg RK, Quinn JF (1986) The genetic control and consequences of kin recognition by the larvae of a colonial marine invertebrate. Nature 322:456–459

    Article  Google Scholar 

  • Hirose E, Saito Y, Watanabe H (1988) A new type of the manifestation of colony specificity in the compound ascidian, Botrylloides violaceus Oka. Biol Bull (Woods Hole) 175:240–245

    Article  Google Scholar 

  • Hirose E, Saito Y, Watanabe H (1990) Allogeneic reaction induced by cut surface contact in the compound ascidian, Botrylloides simodensis. Invertebr Reprod Dev 17:159–164

    Article  Google Scholar 

  • Lambert C, Lambert G (2003) Persistence and differential distribution of nonindigenous ascidians in harbors of the Southern California Bight. Mar Ecol Prog Ser 259:145–161

    Article  Google Scholar 

  • Litman GW (2006) How Botryllus chooses to fuse. Immunity 25:13–15

    Article  CAS  Google Scholar 

  • Mukai H, Watanabe H (1975) Distribution of fusion incompatibility types in natural populations of the compound ascidian Botryllus primigenus. Proc Jpn Acad Sci 51:44–47

    Article  Google Scholar 

  • Paz G, Douek J, Mo C, Goren M, Rinkevich B (2003) Genetic structure of Botryllus schlosseri (Tunicata) populations from the Mediterranean coast of Israel. Mar Ecol Prog Ser 250:153–162

    Article  CAS  Google Scholar 

  • Rinkevich B (2002) The colonial urochordate Botryllus schlosseri: from stem cells and natural tissue transplantation to issues in evolutionary ecology. Bioessays 24:730–740

    Article  Google Scholar 

  • Rinkevich B (2004) Primitive immune systems: are your ways my ways? Immunol Rev 198:25–35

    Article  Google Scholar 

  • Rinkevich B (2005) Rejection patterns in botryllid ascidian immunity: the first tier of allorecognition. Can J Zool 83:101–121

    Article  CAS  Google Scholar 

  • Rinkevich B, Shapira M (1999) Multi-partner urochordate chimeras outperform two-partner chimerical entities. Oikos 87:315–320

    Article  Google Scholar 

  • Rinkevich B, Weissman IL (1987) The fate of Botryllus (Ascidiacea) larvae cosettled with parental colonies: beneficial or deleterious consequences? Biol Bull (Woods Hole) 173:474–488

    Article  Google Scholar 

  • Rinkevich B, Weissman IL (1991) Interpopulational allogeneic reactions in the colonial protochordate Botryllus schlosseri. Int Immunol 3:1265–1272

    Article  CAS  Google Scholar 

  • Rinkevich B, Weissman IL (1992a) Incidents of rejection and indifference in Fu/HC incompatible protochordate colonies. J Exp Zool 263:105–111

    Article  CAS  Google Scholar 

  • Rinkevich B, Weissman IL (1992b) Chimeras vs. genetically homogeneous individuals: potential fitness costs and benefits. Oikos 63:119–124

    Article  Google Scholar 

  • Rinkevich B, Shapira M, Weissman IL, Saito Y (1992) Allogeneic responses between three remote populations of the cosmopolitan ascidian Botryllus schlosseri. Zool Sci (Tokyo) 9:989–994

    Google Scholar 

  • Rinkevich B, Porat R, Goren M (1995) Allorecognition elements on a urochordate histocompatibility locus indicate unprecedented extensive polymorphism. Proc R Soc Lond B Biol Sci 259:319–324

    Article  Google Scholar 

  • Sabbadin A (1955) Osservazioni sullo sviluppo, l’accrescimento e la riproduzione di Botryllus schlosseri (Pallas) in condizioni di laboratorio. Boll Zool 22:243–263

    Article  Google Scholar 

  • Sabbadin A (1977) Linkage between two loci controlling colour polymorphism in the colonial ascidian, Botryllus schlosseri. Experientia (Basel) 33:876–877

    Article  Google Scholar 

  • Stoner DS, Weissman IL (1996) Somatic and germ cell parasitism in a colonial ascidian: possible role for a highly polymorphic allorecognition system. Proc Natl Acad Sci U S A 93:15254–15259

    Article  CAS  Google Scholar 

  • Tsukamoto S, Kato H, Hirota H, Fusetani N (1999) A larval metamorphosis-inducing substance in the ascidian Halocynthia roretzi. Eur J Biochem 264:785–789

    Article  CAS  Google Scholar 

  • Weissman IL, Saito Y, Rinkevich B (1990) Allorecognition histocompatibility in a protochordate species: is the relationship to MHC somatic or structural? Immunol Rev 113:227–241

    Article  CAS  Google Scholar 

  • Winston JE, Jackson JBC (1984) Ecology of cryptic coral reef communities. IV. Community development and life histories of encrusting cheilostome bryozoa. J Exp Mar Biol Ecol 76:1–21

    Article  Google Scholar 

  • Yund PO, Felgarden M (1992) Rapid proliferation of historecognition alleles in populations of a colonial ascidian. J Exp Zool 263:442–452

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank A. H. Powell and two anonymous reviewers for their comments on this manuscript. E. L. Westerman was funded by a National Estuarine Research Reserve Grant from the National Oceanographic and Atmospheric Administration’s Office of Ocean and Coastal Resource Management.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Erica L. Westerman.

Additional information

Communicated by J. P. Grassle.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Westerman, E.L., Dijkstra, J.A. & Harris, L.G. High natural fusion rates in a botryllid ascidian. Mar Biol 156, 2613–2619 (2009). https://doi.org/10.1007/s00227-009-1287-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-009-1287-x

Keywords

Navigation