Skip to main content

Advertisement

SpringerLink
Log in

Pattern of settlement and natural chimerism in the colonial urochordate Botryllus schlosseri

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Colonies of the cosmopolitan urochordate Botryllus schlosseri that share one or both alleles at a single allorecognition locus (Fu/HC) and come into tissue contacts, may fuse and form a mixed entity, a chimera. Botryllus populations worldwide exhibit unprecedented extensive polymorphism at this locus, a result that restricts fusions to kin encounters. This study aims to compare spatiotemporal configurations in source and introduced B. schlosseri populations, residing on natural and man-made substrata, respectively. By using four microsatellite loci, we tested genetic consanguinity of colonies settled naturally along spatial vectors on both, natural (native populations) and man-made (introduced) substrates. Four populations were studied. Results revealed that B. schlosseri colonies, on both substrate types, assemble in groups of relatives that share similar microsatellite profiles. We suggest that this pattern of settlement promotes the formation of chimeras, which evoke conflicting interactions: cooperation between different somatic cell lines that constitute the colonial soma and competition between germ cells that inhabit the chimera gonads. Under natural conditions, the chimera may allow genetic flexibility that depends on joint genomic fitness of its partners. This is probably one of the life history characteristics that led to the worldwide distribution success of this species.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Ben-Shlomo R, Douek J, Rinkevich B (2001) Heterozygote deficiency and chimerism in remote populations of a colonial ascidian from New Zealand. Mar Ecol Prog Ser 209:109–117

    Article  Google Scholar 

  • Ben-Shlomo R, Paz G, Rinkevich B (2006) Post glacial period and recent invasions shape population genetics of botryllid ascidians along European Atlantic coasts. Ecosystems 9:1118–1127

    Article  Google Scholar 

  • Berrill NJ (1950) The Tunicata. Bernard Quaritch Ltd., London

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chadwick-Furman NE, Rinkevich B (1994) A complex allorecognition system in a reef-building coral: Delayed responses, reversals and nontransitive hierarchies. Coral Reefs 13:57–63

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Connell JH (1985) The consequences of variation in initial settlement versus post-settlement mortality in rocky intertidal communities. J Exp Mar Biol Ecol 93:11–45

    Article  Google Scholar 

  • De Tomaso AW, Weissman IL (2004) Evolution of a protochordate allorecognition locus. Science 303:977

    Article  PubMed  Google Scholar 

  • Frank SA (2003) Perspective: Repression of competition and the evolution of cooperation. Evolution 57:693–705

    PubMed  Google Scholar 

  • Giraud T, Pedersen JS, Keller L (2002) Evolution of supercolonies: The Argentine ants of southern Europe. Proc Natl Acad Sci USA 99:6075–6079

    Article  PubMed  CAS  Google Scholar 

  • Giraud T, Blatrix R, Poteaux C, Solignac M, Jaisson P (2001) High genetic relatedness among nestmate queens in the polygynous ponerine ant Gnamptogenys striatula in Brazil. Behav Ecol Sociobiol 49:128–134

    Article  Google Scholar 

  • Grosberg RK (1981) Competitive ability influences habitat choice in marine invertebrates. Nature 290:700–702

    Article  Google Scholar 

  • Grosberg RK (1987) Limited dispersal and proximity-dependent mating success in the sessile colonial ascidian Botryllus schlosseri. Evolution 41:372–384

    Article  Google Scholar 

  • Grosberg RK (1988) The evolution of allorecognition specificity in clonal invertebrates. Quarterly Rev Biol 63:377–412

    Article  Google Scholar 

  • Grosberg RK, Hart MW (2000) Mate selection and the evolution of highly polymorphic self/nonself recognition genes. Science 289:2111–2114

    Article  PubMed  CAS  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 

  • Grosberg RK, Quinn JF (1989) The evolution of aggression based on allorecognition specificity. Evolution 43:504–515

    Article  Google Scholar 

  • Hart MW, Grosberg RK (1999) Kin interactions in a colonial hydrozoan (Hydractinia symbiolongicarpus): population structure on a mobile landscape. Evolution 53:793–805

    Article  Google Scholar 

  • Johnson CR, Seinen I (2002) Selection for restraint in competitive ability in spatial competition systems. Proc R Soc Lond B 269:655– 663

    Article  Google Scholar 

  • Lambert CC, Lambert G (1998) Non-indigenous ascidians in southern California harbors and marinas. Mar Biol 130:675–688

    Article  Google Scholar 

  • Lynch M (1990) The similarity index and DNA fingerprinting. Mol Biol Evol 7:478–484

    PubMed  CAS  Google Scholar 

  • Osman RW, Whitlatch RB (1995) The influence of resident adults on larval settlement: experiments with four species of ascideans. J Exp Mar Biol Ecol 190:199–220

    Article  Google Scholar 

  • Oka K, Watanabe H (1960) Problems of colony specificity in compound ascidian. Bull Mar Biol Stat Asamushi 10:153–155

    Google Scholar 

  • Pancer Z, Gershon H, Rinkevich B (1995) Coexistence and possible parasitism of somatic and germ cell lines in chimeras of the colonial urochordate Botryllus schlosseri. Biol Bull 189:106–112

    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 

  • Pedersen JS, Krieger MJB, Vogel V, Giraud T, Keller L (2006) Native Supercolonies of Unrelated Individuals In The Invasive Argentine Ant. Evolution 60: 782–791

    PubMed  Google Scholar 

  • Pineda J, Caswell H (1997) Dependence of settlement rate on suitable substrate area. Mar Biol 129:541–548

    Article  Google Scholar 

  • Raymond ML, Rousset F (1995) An exact test for population differentiation. Evolution 49: 1280–1283

    Article  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  PubMed  Google Scholar 

  • Rinkevich B (2004) Will two walk together, except they have agreed? J Evol Biol 17:1178–1179

    Article  PubMed  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 173:474–488

    Article  Google Scholar 

  • Rinkevich B, Yankelevich I (2004) Environmental split between germ cell parasitism and somatic cell synergism in chimeras of a colonial urochordate. J Exp Biol 207:3531–3536

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Sabbadin A (1962) La basi genetische della capacita di fusione fra colonie in Botryllus schlosseri (Ascidiacea). Atti Accad Naz Lincei Rc 32:1031–1035

    Google Scholar 

  • Scofield VL, Schlumpberger JM, West LA, Weissman IL (1982) Protochordate allorecognition is controlled by a MHC-like gene system. Nature 295:499–502

    Article  PubMed  CAS  Google Scholar 

  • Sommerfeldt AD, Bishop JDD, Wood CA (2003) Chimerism following fusion in a clonal ascidian (Urochordata). Biol J Linn Soc 79:183–192

    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 USA 93:15254–15259

    Article  PubMed  CAS  Google Scholar 

  • Stoner DS, Rinkevich B, Weissman IL (1999) Heritable germ and somatic cell lineage competitions in chimeric colonial protochordates. Proc Natl Acad Sci USA 96:9148–9153

    Article  PubMed  CAS  Google Scholar 

  • Stoner DS, Ben-Shlomo R, Rinkevich B, Weisman IL (2002) Genetic Variability of Botryllus schlosseri invasions to the East and West Coasts of USA. Mar Ecol Prog Ser 243:93–100

    Article  Google Scholar 

  • Strassmann JE, Colin RH, Queller DC, Turillazzi S, Cervo R, Davis SK, Goodnight KF (1989) Genetic relatedness in primitively eusocial wasps. Nature 342:268–269

    Article  Google Scholar 

  • Thorne BL (1982) Multiple primary queens in termites: phyletic distribution, ecological context, and a comparison to polygyny in Hymenoptera. In: Breed MD, Michener CD, Evans HE (eds) The Biology of social insects. Westview Press, Boulder, Colorado, pp 206–211

    Google Scholar 

  • Tschinkel WR (1993) Resource allocation, brood reduction and cannibalism during colony founding in the fire ant, Solenopsis invicta. Behav Ecol Sociobiol 33:209–233

    Article  Google Scholar 

  • Tsutsui ND, Suarez AV, Grosberg RK (2003) Genetic diversity, asymmetrical aggression, and recognition in a widespread invasive species. Proc Natl Acad Sci USA 100:1078–1083

    Article  PubMed  CAS  Google Scholar 

  • Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of an invasive species. Proc Natl Acad Sci USA 97:5948–5953

    Article  PubMed  CAS  Google Scholar 

  • Van Name WG (1945) The North and South American ascidians. Bull Am Museum Nat Hist 84:220–222

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yund PO, O’Neil PG (2000) Microgeographic genetic differentiation in a colonial ascidian (Botryllus schlosseri) population. Mar Biol 137:583–588

    Article  Google Scholar 

Download references

Acknowledgements

We would like to express our thanks to the anonymous referees, whose helpful suggestions contributed significantly to this study. The work was supported by grants from the EC Marine Genomics Network of Excellence, Israel Science Foundation (550/06) and from the US-Israel Bi-National Foundation (2003–010).

Author information

Authors and Affiliations

  1. Department of Biology, University of Haifa – Oranim, Tivon, 36006, Israel

    Rachel Ben-Shlomo

  2. Department of Evolution, Systematics and Ecology and Department of Statistics, The Hebrew University of Jerusalem, Jerusalem, 91904, Israel

    Uzi Motro

  3. Israel Oceanography and Limnological Research, National Institute of Oceanography, Tel Shikmona, PO Box 8030, Haifa, 31080, Israel

    Guy Paz & Baruch Rinkevich

Authors
  1. Rachel Ben-Shlomo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Uzi Motro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guy Paz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Baruch Rinkevich
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rachel Ben-Shlomo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ben-Shlomo, R., Motro, U., Paz, G. et al. Pattern of settlement and natural chimerism in the colonial urochordate Botryllus schlosseri . Genetica 132, 51–58 (2008). https://doi.org/10.1007/s10709-007-9148-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-007-9148-3

Keywords

Search

Navigation