High potential for formation and persistence of chimeras following aggregated larval settlement in the broadcast spawning coral, Acropora millepora

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1729, 2012, Pages 699-708

  Puill Stephan, E ^a,b,c   van Oppen, M J H ^b   Pichavant Rafini, K ^c   Willis, B L ^a  

^a JAMES COOK UNIVERSITY   (Australia)

^b AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^c UNIVERSITÉ EUROPÉENNE DE BRETAGNE   (France)

Author keywords

Acropora millepora; Chimera; Corals; Microsatellites

Indexed keywords

AGGREGATION BEHAVIOR; CORAL REEF; EVOLUTIONARILY STABLE STRATEGY; GENETIC MARKER; GENOTYPE; JUVENILE; LARVAL SETTLEMENT; LIFE HISTORY TRAIT; MARINE ECOSYSTEM; MOVEMENT; SESSILE SPECIES; SPAWNING; SURVIVAL; VULNERABILITY;

ACROPORA MILLEPORA; ANTHOZOA; INVERTEBRATA;

EID: 84855657203     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.1035     Document Type: Article

References (59)

1. Rinkevich, B. & Weissman, I. L. 1987 Chimeras in colonial invertebrates: a synergistic symbiosis or somatic-and germ-cell parasitism? Symbiosis 4, 117-134.
2. Buss, L.W. 1982 Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc. Natl Acad. Sci. USA 79, 5337-5341. (doi:10.1073/pnas.79.17.5337)
3. Rinkevich, B. 1998 Immunology of human implantation: from the invertebrates' point of view. Hum. Reprod. 13, 455-459. (doi:10.1093/humrep/13.2.455)
4. Rinkevich, B. 2001 Human natural chimerism: an acquired character or a vestige of evolution? Hum. Immunol. 62, 651-657. (doi:10.1016/S0198-8859(01) 00249-X)
5. Santelices, B. 2004 Mosaicism and chimerism as components of intraorganismal genetic heterogeneity. J. Evol. Biol. 17, 1187-1188. (doi:10.1111/j.1420-9101.2004.00813.x)
6. Hughes, R. N. 1989 A functional biology of clonal animals. New York, NY: Chapman and Hall.
7. Sommerfeldt, A. D., Bishop, J. D. D. & Wood, C. A. 2003 Chimerism following fusion in a clonal ascidian (Urochordata). Biol. J. Linn. Soc. 79, 182-192. (doi:10. 1046/j.1095-8312.2003.00179.x)
8. Keough, M. J. 1984 Kin-recognition and the spatial distribution of larvae of the Bryozoan Bugula neritina (L.). Evolution 38, 142-147. (doi:10.2307/2408553)
9. Sommerfeldt, A. D. & Bishop, J. D. D. 1999 Random amplified polymorphic DNA (RAPD) analysis reveals extensive natural chimerism in a marine protochordate. Mol. Ecol. 8, 885-890. (doi:10.1046/j.1365-294X.1999. 00625.x)
10. 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. (doi:10.3354/meps209109)
11. Rinkevich, B. 2005 Natural chimerism in colonial urochordates. J. Exp. Mar. Biol. Ecol. 322, 93-109. (doi:10.1016/j.jembe.2005.02.020)
12. 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. (doi:10.1007/s10709-007-9148-3)
13. Grosberg, R. K. 1988 The evolution of allorecognition specificity in clonal invertebrates. Q. Rev. Biol. 63, 377-412. (doi:10.1086/416026)
14. Heyward, A. J. & Stoddart, J. A. 1985 Genetic structure of two species of Montipora on a patch reef: conflicting results from electrophoresis and histocompatibility. Mar. Biol. 85, 117-121. (doi:10.1007/BF00397429)
15. Stoddart, J. A., Ayre, D. J., Willis, B. L. & Heyward, A. J. 1985 Self-recognition in sponges and corals? Evolution 39, 461-463. (doi:10.2307/2408378)
16. Willis, B. L. & Ayre, D. J. 1985 Asexual reproduction and genetic determination of growth form in the coral Pavona cactus: biochemical genetic and immunogenic evidence. Oecologia 65, 516-525. (doi:10.1007/BF00379666)
17. Amar, K. O., Chadwick, N. E. & Rinkevich, B. 2008 Coral kin aggregations exhibit mixed allogeneic reactions and enhanced fitness during early ontogeny. BMC Evol. Biol. 8, 126-136. (doi:10.1186/1471-2148-8-126)
18. Neigel, J. E. & Avise, J. C. 1983 Clonal diversity and population structure in a reef-building coral, Acropora cervicornis: self-recognition analysis and demographic interpretation. Evolution 37, 437-453. (doi:10.2307/2408259)
19. Hidaka, M. 1985 Nematocyst discharge, histoincompatibility, and the formation of sweeper tentacles in the coral Galaxea fascicularis. Biol. Bull. 168, 350-358. (doi:10.2307/1541517)
20. Hidaka, M. 1985 Tissue compatibility between colonies and between newly settled larvae of Pocillopora damicornis. Coral Reefs 4, 111-116. (doi:10.1007/BF00300869)
21. Chadwick-Furman, N. & Rinkevich, B. 1994 A complex allorecognition system in a reef-building coral: delayed responses, reversals and nontransitive hierarchies. Coral Reefs 13, 57-63. (doi:10.1007/BF00426436)
22. Frank, U. & Rinkevich, B. 1994 Nontransitive patterns of historecognition phenomena in the Red Sea hydrocoral Millepora dichotoma. Mar. Biol. 118, 723-729. (doi:10. 1007/BF00347521)
23. Hidaka, M., Yurugi, K., Sunagawa, S. & Kinzie III, R. A. 1997 Contact reactions between young colonies of the coral Pocillopora damicornis. Coral Reefs 16, 13-20. (doi:10.1007/s003380050054)
24. 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. B 264, 99-104. (doi:10.1098/rspb.1997.0015)
25. Frank, U. & Rinkevich, B. 2001 Alloimmune memory is absent in the Red Sea hydrocoral Millepora dichotoma. J. Exp. Zool. 291, 25-29. (doi:10.1002/jez.3)
26. Barki, Y., Gateno, D., Graur, D. & Rinkevich, B. 2002 Softcoral natural chimerism: a window in ontogeny allows the creation of entities comprised of incongruous parts. Mar. Ecol. Prog. Ser. 231, 91-99. (doi:10.3354/meps231091)
27. Rinkevich, B. 2004 Allorecognition and xenorecognition in reef corals: a decade of interactions. Hydrobiologia 530/531, 443-450. (doi:10.1007/s10750-004-2686-0)
28. 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, 115-123. (doi:10.3354/meps286115)
29. Puill-Stephan, E., Willis, B. L., van Herwerden, L. & van Oppen, M. J. H. 2009 Chimerism in wild adult populations of the broadcast spawning coral Acropora millepora on the Great Barrier Reef. PLoS ONE 4, e7751. (doi:10.1371/journal.pone.0007751)
30. Rinkevich, B. 2004 Will two walk together, except they have agreed? Amos 3:3. J. Evol. Biol. 17, 1178-1179. (doi:10.1111/j.1420-9101.2004.00809.x)
31. Santelices, B. 1999 How many kinds of individuals are there? Trends Ecol. Evol. 14, 152-155. (doi:10.1016/ S0169-5347(98)01519-5)
32. Strassmann, J. E. & Queller, D. C. 2004 Genetic conflicts and intercellular heterogeneity. J. Evol. Biol. 17, 1189-1191. (doi:10.1111/j.1420-9101.2004.00814.x)
33. Babcock, R. C., Bull, G. D., Harrison, P. L., Heyward, A. J., Oliver, J. K., Wallace, C. C. & Willis, B. L. 1986 Synchronous spawnings of 105 scleratinian coral species on the Great Barrier Reef. Mar. Biol. 90, 379-394. (doi:10.1007/BF00428562)
34. Oliver, J. K. & Willis, B. L. 1987 Coral-spawn slicks in the Great Barrier Reef: preliminary observations. Mar. Biol. 94, 521-529. (doi:10.1007/BF00431398)
35. Siegel, D. A., Mitarai, S., Costello, C. J., Gaines, S. D., Kendall, B. E., Warner, R. R. & Winters, K. B. 2008 The stochastic nature of larval connectivity among nearshore marine populations. Proc. Natl Acad. Sci. USA 105, 8974-8979. (doi:10.1073/pnas.0802544105)
36. Graham, E. M., Baird, A. H. & Connolly, S. R. 2008 Survival dynamics of scleractinian coral larvae and implications for dispersal. Coral Reefs 27, 529-539. (doi:10. 1007/s00338-008-0361-z)
37. Heyward, A. J. & Negri, A. P. 2010 Plasticity of larval pre-competency in response to temperature: observations on multiple broadcast spawning coral species. Coral Reefs 29, 631-636. (doi:10.1007/s00338-009-0578-5)
38. van Oppen, M. J.H., Underwood, J.N., Muirhead, A.N. & 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, 436-438. (doi:10.1111/j.1471-8286.2006.01610.x)
39. Wilson, K. et al. 2002 Genetic mapping of the black tiger shrimp Penaeus monodon with amplified fragment length polymorphism. Aquaculture 204, 297-309. (doi:10. 1016/S0044-8486(01)00842-0)
40. Kuick, R. D., Neel, J. V., Strahler, J. R., Chu, E. H. Y., Bargal, R., Fox, D. A. & Hanash, S. M. 1992 Similarity of spontaneous germinal and in vitro somatic cell mutation rates in humans: implications for carcinogenesis and for the role of exogenous factors in 'spontaneous' germinal mutagenesis. Proc. Natl Acad. Sci. USA 89, 7036-7040. (doi:10.1073/pnas.89.15.7036)
41. Loeb, L. A. 1991 Mutator phenotype may be required for multistage carcinogenesis. Cancer Res. 28, 491-511.
42. Litchen, M. & Haber, J. E. 1989 Position effects in ectopic and allelic mitotic recombination in Saccharomyces cerevisiae. Genetics 123, 261-268.
43. Orive, M. E. 2001 Somatic mutations in organisms with complex life histories. Theor. Popul. Biol. 59, 235-249. (doi:10.1006/tpbi.2001.1515)
44. Peakall, R. & Smouse, P. E. 2006 GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6, 288-295. (doi:10. 1111/j.1471-8286.2005.01155.x)
45. Queller, D. C. & Goodnight, K. F. 1989 Estimating relatedness using genetic markers. Evolution 43, 258-275. (doi:10.2307/2409206)
46. Lewis, J. B. 1974 Settlement and growth factors influencing the contagious distribution of some Atlantic reef corals. In Proc. of the Second Int. Coral Reef Symp. vol. 2 (eds A. M. Cameron, B. M. Campbell, A. B. Cribb, R. Endean, J. S. Jell, O. A. Jones, P. Mather & F. H. Talbot), pp. 201-206. Brisbane, Australia: Great Barrier Reef Committee.
47. Smith, S. R. 1997 Patterns of coral recruitment, recruitment and juvenile mortality with depth at Conch Reef, Florida. In 8th Int. Coral Reef Symp. vol. 2 (eds H. A. Lessios & I. G. Macintyre), pp. 1197-1202. Panama, FL: Smithsonian Tropical Research Institute.
48. Zilberberg, C. & Edmunds, P. J. 2001 Competition among small colonies of Agaricia: the importance of size asymmetry in determining competitive outcome. Mar. Ecol. Prog. Ser. 221, 125-133. (doi:10.3354/meps221125)
49. Sammarco, P. W. 1982 Echinoid grazing as a structuring force in coral communities: whole reef manipulations. J. Exp. Mar. Biol. Ecol. 61, 31-55. (doi:10.1016/0022-0981(82)90020-X)
50. Jackson, J. B. C. 1979 Morphological strategies of sessile animals. In Biology and systematics of colonial organisms (eds G. Larwood & B. R. Rosen), pp. 499-555. London, UK: Academic Press.
51. Grosberg, R. K. & Quinn, J. F. 1986 The genetic control and the consequences of kin recognition by the larvae of a colonial marine invertebrate. Nature 322, 456-459. (doi:10.1038/322456a0)
52. Willis, B. L., Babcock, R. C., Harrison, P. L., Oliver, J. K. & Wallace, C. C. 1985 Patterns in the mass spawning of corals on the Great Barrier Reef from 1981 to 1984. In Proc. of the Fifth Int. Coral Reef Congress, vol. 4 (eds C. Gabrie & B. Salvat), pp. 343-348. Penang, Malaysia: The WorldFish Center.
53. Babcock, R. C. & Heyward, A. J. 1986 Larval development of certain gamete-spawning scleractinian corals. Coral Reefs 5, 111-116. (doi:10.1007/BF00298178)
54. Miller, K. & Mundy, C. 2003 Rapid settlement in broadcast spawning corals: implications for larval dispersal. Coral Reefs 22, 99-106. (doi:10.1007/s00338-003-0290-9)
55. Wilson, A. C. C. & Grosberg, R. K. 2004 Ontogenetic shifts in fusion-rejection thresholds in a colonial marine hydrozoan, Hydractinia symbiolongicarpus. Behav. Ecol. Sociobiol. 57, 40-49. (doi:10.1007/s00265-004-0831-4)
56. Hughes, R.N., Manriquez, P. H., Morley, S., Craig, S. F. & Bishop, J. D. D. 2004 Kin or self-recognition? Colonial fusibility of the bryozoan Celleporella hyalina. Evol. Dev. 6, 431-437. (doi:10.1111/j.1525-142X.2004.04051.x)
57. Abrego, D., van Oppen, M. J. H. & Willis, B. L. 2009 Onset of algal endosymbiont specificity varies among closely related species of Acropora corals during early ontogeny. Mol. Ecol. 18, 3532-3543. (doi:10.1111/j. 1365-294X.2009.04276.x)
58. Chadwick-Furman, N. E. & Weissman, I. L. 2003 Effects of allogeneic contact on life-history traits of the colonial ascidians Botryllus schlosseri in Monterey Bay. Biol. Bull. 205, 133-143. (doi:10.2307/1543234)
59. Jackson, J. B. C. & Hughes, T. P. 1985 Adaptive strategies of coral reef invertebrates. Am. Sci. 73, 265-274.