Coral Reefs

, Volume 31, Issue 4, pp 1019–1028 | Cite as

Allorecognition maturation in the broadcast-spawning coral Acropora millepora

  • E. Puill-Stephan
  • B. L. Willis
  • D. Abrego
  • J.-B. Raina
  • M. J. H. van Oppen


Many sessile marine invertebrates discriminate self from non-self with great precision, but maturation of allorecognition generally takes months to develop in juveniles. Here, we compare the development of allorecognition in full-sibling, half-sibling and non-sibling contact reactions between newly settled juveniles of the broadcast-spawning coral Acropora millepora on the Great Barrier Reef (Australia). Absence of a rejection response showed that A. millepora lacks a mature allorecognition system in the first 2 months post-settlement. From thereon, incompatibilities were observed between juveniles, their level of relatedness (i.e. full-, half- and non-sibling status) governing the rate of allorecognition maturation. All contact reactions between non-siblings resulted in rejections by 3 months post-settlement, whereas the expression of allorecognition took at least 5 months between half-siblings and longer than 13 months for some full-siblings. Approximately 74 % of fused full-siblings (n = 19) persisted as chimeras at 11 months, thus maturation of allorecognition in this spawning coral appeared to be slower (>13 months) than in brooding corals (~4 months). We hypothesize that late maturation of allorecognition may contribute to flexibility in Symbiodinium uptake in corals with horizontal transmission, and could allow fusions and chimera formation in early ontogeny, which potentially enable rapid size increase through fusion.


Allorecognition Immunity Self–non-self-recognition Acropora millepora Corals 



We thank Andrew Muirhead, Lesa Peplow, Francois Seneca, Yossi Loya and Andrew Negri for their very precious and enthusiastic advice and help in the field and in the laboratory. Funding was provided by an Australian Research Council DP grant to BW and MvO.


  1. Abrego D, van Oppen MJH, Willis BL (2009) Onset of algal endosymbiont specificity varies among closely related species of Acropora corals during early ontogeny. Mol Ecol 18:3532–3543PubMedCrossRefGoogle Scholar
  2. Amar KO, Rinkevich B (2010) Mounting of erratic histoincompatible responses in hermatypic corals: a multi-year interval comparison. J Exp Biol 213:535–540PubMedCrossRefGoogle Scholar
  3. Amar KO, Chadwick NE, Rinkevich B (2008) Coral kin aggregations exhibit mixed allogeneic reactions and enhanced fitness during early ontogeny. BMC Evol Biol 8:126–136PubMedCrossRefGoogle Scholar
  4. Anthony KRN, Ridd PV, Orpin AR, Larcombe P, Lough J (2004) Temporal variation of light availability in coastal benthic habitats: effects of clouds, turbidity, and tides. Limnol Oceanogr 49:2201–2211CrossRefGoogle Scholar
  5. Babcock RC, Mundy C (1996) Coral recruitment: consequences of settlement choice for early growth and survivorship in two scleractinians. J Exp Mar Biol Ecol 206:179–201CrossRefGoogle Scholar
  6. Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, Willis BL (1986) Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef. Mar Biol 90:379–394CrossRefGoogle Scholar
  7. Barki Y, Gateño D, Graur D, Rinkevich B (2002) Soft-coral natural chimerism: a window in ontogeny allows the creation of entities comprised of incongruous parts. Mar Ecol Prog Ser 231:91–99CrossRefGoogle Scholar
  8. 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 209:109–117CrossRefGoogle Scholar
  9. Ben-Shlomo R, Motro U, Paz G, Rinkevich B (2008) Pattern of settlement and natural chimerism in the colonial urochordate Botryllus schlosseri. Genetica 132:51–58PubMedCrossRefGoogle Scholar
  10. Frank U, Oren U, Loya Y, Rinkevich B (1997) Alloimmune maturation in the coral Stylophora pistillata is achieved through three distinctive stages, 4 months post-metamorphosis. Proc R Soc Lond Ser B: Biol Sci 264:99–104CrossRefGoogle Scholar
  11. Grosberg RK (1988) Life-history variation within a population of the colonial ascidian Botryllus schlosseri. I. The genetic control and environmental control of seasonal variation. Evolution 42:900–920CrossRefGoogle Scholar
  12. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Coral reefs. Elsevier, Amsterdam, pp 133–207Google Scholar
  13. Hart MW, Grosberg RK (1999) Kin interactions in a colonial hydrozoan (Hydractinia symbiolongicarpus): population structure on a mobile landscape. Evolution 53:793–805CrossRefGoogle Scholar
  14. Heyward AJ, Stoddart JA (1985) Genetic structure of two species of Montipora on a patch reef: conflicting results from electrophoresis and histocompatibility. Mar Biol 85:117–121CrossRefGoogle Scholar
  15. Hidaka M, Yurugi K, Sunagawa S, Kinzie RA III (1997) Contact reactions between young colonies of the coral Pocillopora damicornis. Coral Reefs 16:13–20CrossRefGoogle Scholar
  16. Jackson JBC (1986) Modes of dispersal of clonal benthic invertebrates: consequences for species distributions and genetic structure of local populations. Bull Mar Sci 39:588–606Google Scholar
  17. Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494PubMedCrossRefGoogle Scholar
  18. Nozawa Y, Hirose M (2011) When does the window close?: The onset of allogeneic fusion 2-3 years post-settlement in the scleractinian coral, Echinophyllia aspera. Zool Stud 50:396Google Scholar
  19. Nozawa Y, Loya Y (2005) Genetic relationship and maturity state of the allorecognition system affect contact reactions in juvenile Seriatopora corals. Mar Ecol Prog Ser 286:115–123CrossRefGoogle Scholar
  20. Nürnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266PubMedCrossRefGoogle Scholar
  21. Puill-Stephan E, Willis BL, van Herwerden L, van Oppen MJH (2009) Chimerism in wild adult populations of the broadcast spawning coral Acropora millepora on the Great Barrier Reef. PLoS ONE 4:e7751PubMedCrossRefGoogle Scholar
  22. Puill-Stephan E, van Oppen MJH, Pichavant-Rafini K, Willis BL (2012) High potential for formation and persistence of chimeras following aggregated larval settlement in the broadcast spawning coral, Acropora millepora. Proc R Soc Lond Ser B: Biol Sci 279:699–708CrossRefGoogle Scholar
  23. Raymundo LJ, Maypa AP (2004) Getting bigger faster: mediation of size-specific mortality via fusion in juvenile coral transplants. Ecol Appl 14:281–295CrossRefGoogle Scholar
  24. Resing JM, Ayre DJ (1985) The usefulness of the tissue grafting bioassay as an indicator of clonal identity in scleractinian corals (Great Barrier Reef—Australia). Proc 5th Int Coral Reef Cong:75–81Google Scholar
  25. Rinkevich B (2004) Will two walk together, except they have agreed? Amos 3 : 3. J Evol Biol 17:1178–1179PubMedCrossRefGoogle Scholar
  26. Rinkevich B (2005) Natural chimerism in colonial urochordates. J Exp Mar Biol Ecol 322:93–109CrossRefGoogle Scholar
  27. Rinkevich B, Weissman IL (1987) Chimeras in colonial invertebrates: a synergistic symbiosis or somatic- and germ-cell parasitism? Symbiosis 4:117–134Google Scholar
  28. Santelices B (1999) How many kinds of individuals are there? Trends Ecol Evol 14:152–155PubMedCrossRefGoogle Scholar
  29. Sommerfeldt AD, Bishop JDD (1999) Random amplified polymorphic DNA (RAPD) analysis reveals extensive natural chimerism in a marine protochordate. Mol Ecol 8:885–890CrossRefGoogle Scholar
  30. Sommerfeldt AD, Bishop JDD, Wood CA (2003) Chimerism following fusion in a clonal ascidian (Urochordata). Biol J Linn Soc 79:182–192CrossRefGoogle Scholar
  31. van Oppen MJH, Underwood JN, Muirhead AN, Peplow L (2007) Ten microsatellite loci for the reef-building coral Acropora millepora (Cnidaria, Scleractinia) from the Great Barrier Reef, Australia. Mol Ecol Notes 7:436–438CrossRefGoogle Scholar
  32. Willis BL, Ayre DJ (1985) Asexual reproduction and genetic determination of growth form in the coral Pavona cactus: biochemical genetic and immunogenic evidence. Oecologia 65:516–525CrossRefGoogle Scholar
  33. Willis BL, Babcock RC, Harrison PL, Oliver JK, Wallace CC (1985) Patterns in the mass spawning of corals on the Great Barrier Reef from 1981 to 1984. Proc 5th Int Coral Reef Congr 4:343–348Google Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • E. Puill-Stephan
    • 1
    • 2
    • 3
    • 4
  • B. L. Willis
    • 2
  • D. Abrego
    • 3
  • J.-B. Raina
    • 1
    • 3
  • M. J. H. van Oppen
    • 2
    • 3
  1. 1.AIMS@JCU, James Cook UniversityTownsvilleAustralia
  2. 2.ARC Centre of Excellence for Coral Reef Studies and School of Marine and Tropical BiologyJames Cook UniversityTownsvilleAustralia
  3. 3.Australian Institute of Marine ScienceTownsville MCAustralia
  4. 4.UFR Sciences et TechniquesORPHY, EA 4324, Université Européenne de Bretagne, Université de BrestBrest cédexFrance

Personalised recommendations