Skip to main content
Log in

Intracolonial genetic variation in the scleractinian coral Seriatopora hystrix

  • Note
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

In recent years, increasing numbers of studies revealed intraorganismal genetic variation, primarily in modular organisms like plants or colonial marine invertebrates. Two underlying mechanisms are distinguished: Mosaicism is caused by somatic mutation, whereas chimerism originates from allogeneic fusion. We investigated the occurrence of intracolonial genetic variation at microsatellite loci in five natural populations of the scleractinian coral Seriatopora hystrix on the Great Barrier Reef. This coral is a widely distributed, brooding species that is at present a target of intensive population genetic research on reproduction and dispersal patterns. From each of 155 S. hystrix colonies, either two or three samples were genotyped at five or six loci. Twenty-seven (~17%) genetically heterogeneous colonies were found. Statistical analyses indicated the occurrence of both mosaicism and chimerism. In most cases, intracolonial variation was found only at a single allele. Our analyses suggest that somatic mutations present a major source of genetic heterogeneity within a single colony. Moreover, we observed large, apparently stable chimeric colonies that harbored clearly distinct genotypes and contrast these findings with the patterns typically observed in laboratory-based experiments. We discuss the error that mosaicism and chimerism introduce into population genetic analyses.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  • 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

    Article  PubMed  Google Scholar 

  • Arnaud-Haond S, Duarte CM, Alberto F, Serrão EA (2007) Standardizing methods to address clonality in population studies. Mol Ecol 16:5115–5139

    Article  PubMed  CAS  Google Scholar 

  • Atoda K (1951) The larva and postlarval development of the reef-building corals. V. Seriatopora hystrix Dana. Sci Rep Tohoku Univ Fourth Ser (Biol) 19:33–39

    Google Scholar 

  • Ayre DJ, Dufty S (1994) Evidence for restricted gene flow in the viviparous coral Seriatopora hystrix on Australia’s Great Barrier Reef. Evolution 48:1183–1201

    Article  Google Scholar 

  • Ayre DJ, Hughes TP (2000) Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia. Evolution 54:1590–1605

    PubMed  CAS  Google Scholar 

  • 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 231:91–99

    Article  Google Scholar 

  • Baums IB, Hughes CR, Hellberg ME (2005) Mendelian microsatellite loci for the Caribbean coral Acropora palmata. Mar Ecol Prog Ser 288:115–127

    Article  CAS  Google Scholar 

  • Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  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 

  • Buss LW (1987) The evolution of individuality. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Carpenter MA, Powell JH, Ishizuka KJ, Palmeri KJ, Rendulic S, De Tomaso AW (2011) Growth and long-term somatic and germline chimerism following fusion of juvenile Botryllus schlosseri. Biol Bull 220:57–70

    PubMed  CAS  Google Scholar 

  • Chen C, Durand E, Forbes F, François O (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Mol Ecol Notes 7:747–756

    Article  Google Scholar 

  • François O, Ancelet S, Guillot G (2006) Bayesian clustering using hidden Markov random fields in spatial population genetics. Genetics 174:805–816

    Article  PubMed  Google Scholar 

  • 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 Biol Sci Ser B 264:99–104

    Article  Google Scholar 

  • Gao H, Williamson S, Bustamante CD (2007) A Markov chain Monte Carlo approach for joint inference of population structure and inbreeding rates from multilocus genotype data. Genetics 176:1635–1651

    Article  PubMed  Google Scholar 

  • Gill DE, Chao L, Perkins SL, Wolf JB (1995) Genetic mosaicism in plants and clonal animals. Annu Rev Ecol Syst 26:423–444

    Article  Google Scholar 

  • Gottlieb B, Beitel LK, Alvarado C, Trifiro MA (2010) Selection and mutation in the “new” genetics: an emerging hypothesis. Hum Genet 127:491–501

    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 

  • 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 

  • Hidaka M (1985) Tissue compatibility between colonies and between newly settled larvae of Pocillopora damicornis. Coral Reefs 4:111–116

    Article  Google Scholar 

  • Hidaka M, Yurugi K, Sunagawa S, Kinzie RA III (1997) Contact reactions between young colonies of the coral Pocillopora damicornis. Coral Reefs 16:13–20

    Article  Google Scholar 

  • Hoffman JI, Amos W (2005) Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion. Mol Ecol 14:599–612

    Article  PubMed  CAS  Google Scholar 

  • Hughes TP, Ayre D, Connell JH (1992) The evolutionary ecology of corals. Trends Ecol Evol 7:292–295

    Article  PubMed  CAS  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  PubMed  CAS  Google Scholar 

  • Hughes RN, Manríquez PH, Morley S, Craig SF, Bishop JDD (2004) Kin or self-recognition? Colonial fusibility of the bryozoan Celleporella hyalina. Evol Dev 6:431–437

    Article  PubMed  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  PubMed  CAS  Google Scholar 

  • Keough MJ (1984) Kin-recognition and the spatial distribution of larvae of the bryozoan Bugula neritina (L.). Evolution 38:142–147

    Article  Google Scholar 

  • Lowe A, Harris S, Ashton P (2004) Ecological genetics: design, analysis,and application. Blackwell Publishing, Oxford

    Google Scholar 

  • Magalon H, Samadi S, Richard M, Adjeroud M, Veuille M (2004) Development of coral and zooxanthella-specific microsatellites in three species of Pocillopora (Cnidaria, Scleractinia) from French Polynesia. Mol Ecol Notes 4:206–208

    Article  CAS  Google Scholar 

  • Maier E, Tollrian R, Nürnberger B (2001) Development of species-specific markers in an organism with endosymbionts: microsatellites in the scleractinian coral Seriatopora hystrix. Mol Ecol Notes 1:157–159

    Article  CAS  Google Scholar 

  • Maier E, Tollrian R, Rinkevich B, Nürnberger B (2005) Isolation by distance in the scleractinian coral Seriatopora hystrix from the Red Sea. Mar Biol 147:1109–1120

    Article  Google Scholar 

  • Maier E, Tollrian R, Nürnberger B (2009) Fine-scale analysis of genetic structure in the brooding coral Seriatopora hystrix from the Red Sea. Coral Reefs 28:751–756

    Article  Google Scholar 

  • Maldonado M (1998) Do chimeric sponges have improved chances of survival? Mar Ecol Prog Ser 164:301–306

    Article  Google Scholar 

  • Monro K, Poore AGB (2009) The potential for evolutionary responses to cell-lineage selection on growth form and its plasticity in a red seaweed. Am Nat 173:151–163

    Article  PubMed  Google Scholar 

  • Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405

    Article  Google Scholar 

  • Noreen AME, Harrison PL, van Oppen MJH (2009) Genetic diversity and connectivity in a brooding reef coral at the limit of its distribution. Proc R Soc Lond B Biol Sci 276:3927–3935

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Ohta T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genet Res 22:201–204

    Article  Google Scholar 

  • Orive ME (2001) Somatic mutations in organisms with complex life histories. Theor Popul Biol 59:235–249

    Article  PubMed  CAS  Google Scholar 

  • Otto SP, Hastings IM (1998) Mutation and selection within the individual. Genetica 102:507–524

    Article  PubMed  Google Scholar 

  • Pineda-Krch M, Lehtilä K (2004) Costs and benefits of genetic heterogeneity within organisms. J Evol Biol 17:1167–1177

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • 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(11):e7751

    Article  PubMed  Google Scholar 

  • Raymundo LJ, Maypa AP (2004) Getting bigger faster: mediation of size-specific mortality via fusion in juvenile coral transplants. Ecol Appl 14:281–295

    Article  Google Scholar 

  • 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 Congr 6:75–81

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Rinkevich B (1996) Bi- versus multichimerism in colonial urochordates: a hypothesis for links between natural tissue transplantation, allogenetics, and evolutionary ecology. Exp Clin Immunogenet 13:61–69

    PubMed  CAS  Google Scholar 

  • Rinkevich B, Loya Y (1983) Intraspecific competitive networks in the Red Sea coral Stylophora pistillata. Coral Reefs 1:161–172

    Article  Google Scholar 

  • Santelices B (2004) Mosaicism and chimerism as components of intraorganismal genetic heterogeneity. J Evol Biol 17:1187–1188

    Article  PubMed  CAS  Google Scholar 

  • Schlötterer C (2000) Evolutionary dynamics of microsatellite DNA. Chromosoma 109:365–371

    Article  PubMed  Google Scholar 

  • Shenk MA, Buss LW (1991) Ontogenetic changes in fusibility in the colonial hydroid Hydractinia symbiolongicarpus. J Exp Zool 257:80–86

    Article  Google Scholar 

  • Sherman CDH (2008) Mating system variation in the hermaphroditic brooding coral, Seriatopora hystrix. Heredity 100:296–303

    Article  PubMed  CAS  Google Scholar 

  • Slavov GT, Howe GT, Gyaourova AV, Birkes DS, Adams WT (2005) Estimating pollen flow using SSR markers and paternity exclusion: accounting for mistyping. Mol Ecol 14:3109–3121

    Article  PubMed  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1994) Biometry, 3rd edn. Freeman, San Francisco

    Google Scholar 

  • Sommerfeldt AD, Bishop JDD (1999) Random amplified polymorphic DNA (RAPD) analysis reveals extensive natural chimerism in a marine protochordate. Mol Ecol 8:885–890

    Article  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 

  • Stimson JS (1978) Mode and timing of reproduction in some common hermatypic corals of Hawaii and Enewetak. Mar Biol 48:173–184

    Article  Google Scholar 

  • Strassmann JE, Queller DC (2004) Genetic conflicts and intercellular heterogeneity. J Evol Biol 17:1189–1191

    Article  PubMed  CAS  Google Scholar 

  • Striewski S (2009) Examination on the intracolonial genetic variation in the scleractinian coral Seriatopora hystrix. Master thesis. Ruhr-Universität Bochum, Germany

  • Taberlet P, Waits LP, Luikart G (1999) Noninvasive genetic sampling: look before you leap. Trends Ecol Evol 14:323–327

    Article  PubMed  Google Scholar 

  • Underwood JN, Souter PB, Ballment ER, Lutz AH, van Oppen MJH (2006) Development of 10 polymorphic microsatellite markers from herbicide-bleached tissues of the brooding pocilloporid coral Seriatopora hystrix. Mol Ecol Notes 6:176–178

    Article  CAS  Google Scholar 

  • Underwood JN, Smith LD, van Oppen MJH, Gilmour JP (2007) Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Mol Ecol 16:771–784

    Article  PubMed  CAS  Google Scholar 

  • Underwood JN, Smith LD, van Oppen MJH, Gilmour JP (2009) Ecologically relevant dispersal of corals on isolated reefs: implications for managing resilience. Ecol Appl 19:18–29

    Article  PubMed  Google Scholar 

  • 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 7:436–438

    Article  Google Scholar 

  • van Oppen MJH, Lutz A, De’ath G, Peplow L, Kininmonth S (2008) Genetic traces of recent long-distance dispersal in a predominantly self-recruiting coral. PLoS ONE 3(10):e3401

    Article  PubMed  Google Scholar 

  • van Oppen MJH, Bongaerts P, Underwood JN, Peplow LM, Cooper TF (2011) The role of deep reefs in shallow reef recovery: an assessment of vertical connectivity in a brooding coral from west and east Australia. Mol Ecol 20:1647–1660

    Article  PubMed  Google Scholar 

  • Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, Townsville

    Google Scholar 

  • Waits JL, Leberg PL (2000) Biases associated with population estimation using molecular tagging. Anim Conserv 3:191–199

    Article  Google Scholar 

  • Willis BL, Ayre DJ (1985) Asexual reproduction and genetic determination of growth form in the coral Pavona cactus: biochemical genetic and immunogenic evidence. Oecologia (Berlin) 65:516–525

    Article  Google Scholar 

Download references

Acknowledgments

This study was funded by the Deutsche Forschungsgemeinschaft (NU 51/5 to BN and RT) and by a HWP grant from the Ludwig Maximilian University. C. Haacke and C. Laforsch provided field assistance. We thank the directors and staff of the Lizard and Heron Island Research Stations for their cooperation. The Great Barrier Reef Marine Park Authority kindly gave us permission to sample S. hystrix. We thank J. M. Jeschke, S. Giessler and C. Mayer for fruitful discussions. Constructive and insightful criticism from K. P. Lampert and the anonymous reviewers greatly improved the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. Maier.

Additional information

Communicated by Biology Editor Dr. Ruth Gates

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 167 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maier, E., Buckenmaier, A., Tollrian, R. et al. Intracolonial genetic variation in the scleractinian coral Seriatopora hystrix . Coral Reefs 31, 505–517 (2012). https://doi.org/10.1007/s00338-011-0857-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-011-0857-9

Keywords

Navigation