Skip to main content
Log in

Isolation by distance in the scleractinian coral Seriatopora hystrix from the Red Sea

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Pelagic dispersal of larvae in sessile marine invertebrates could in principle lead to a homogeneous gene pool over vast distances, yet there is increasing evidence of surprisingly high levels of genetic differentiation on small spatial scale. To evaluate whether larval dispersal is spatially limited and correlated with distance, we conducted a study on the widely distributed, viviparous reef coral Seriatopora hystrix from the Red Sea where we investigated ten populations separated between ~0.150 km and ~610 km. We addressed these questions with newly developed, highly variable microsatellite markers. We detected moderate genetic differentiation among populations based on both F ST and R ST (0.089 vs. 0.136, respectively) as well as considerable heterozygote deficits. Mantel tests revealed isolation by distance effects on a small geographic scale (≤20 km), indicating limited dispersal of larvae. Our data did not reveal any evidence against strictly sexual reproduction among the studied populations.

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
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adjeroud M, Tsuchiya M (1999) Genetic variation and clonal structure in the scleractinian coral Pocillopora damicornis in the Ryukyu Archipelago, southern Japan. Mar Biol 134:753–760

    Article  Google Scholar 

  • Anderson TJC, Su XZ, Roddam A, Day KP (2000) Complex mutations in a high proportion of microsatellite loci from the protozoan parasite Plasmodium falciparum. Mol Ecol 9:1599–1608

    Article  PubMed  CAS  Google Scholar 

  • Atoda K (1951) The larva and postlarval development of the reef-building corals. V. Seriatopora hystrix Dana. The Science Reports of the Tohoku University, Series 4:33–39

    Google Scholar 

  • Ayre DJ (1984) The effects of sexual and asexual reproduction on geographic variation in the sea anemone Actinia tenebrosa. Oecologia 69:222–229

    Article  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, Resing JM (1986) Sexual and asexual production of planulae in reef corals. Mar Biol 90:187–190

    Article  Google Scholar 

  • Ayre DJ, Davis AR, Billingham M, Llorens T, Styan C (1997a) Genetic evidence for contrasting patterns of dispersal in solitary and colonial ascidians. Mar Biol (Berl) 130:51–61

    Article  Google Scholar 

  • Ayre DJ, Hughes, TP, Standish, RJ (1997b) Genetic differentiation, reproductive mode, and gene flow in the brooding coral Pocillopora damicornis along the Great Barrier Reef, Australia. Mar Ecol Prog Ser 159:175–187

    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 

  • Balloux F, Goudet J (2002) Statistical properties of population differentiation estimators under stepwise mutation in a finite island model. Mol Ecol 11:771–783

    Article  PubMed  CAS  Google Scholar 

  • Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165

    Article  PubMed  Google Scholar 

  • Bastidas C, Benzie JAH, Fabricius KE (2002) Genetic differentiation among populations of the brooding soft coral Clavularia koellikeri on the Great Barrier Reef. Coral Reefs 21:233–241

    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 

  • Bohonak AJ (2002) IBD (Isolation by distance): a program for population genetic analyses of isolation by distance. Available from http://www.bio.sdsu.edu/pub/andy/IBD.html

  • Brazeau DA, Harvell CD (1994) Genetic structure of local populations and divergence between growth form in a clonal invertebrate, the Caribbean octocoral Briareum asbestinum. Mar Biol 119:53–60

    Article  Google Scholar 

  • Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5:453–455

    Article  PubMed  CAS  Google Scholar 

  • Callen DF, Thompson, AD, Shen Y, Phillips HA, Richards RI, Mulley JC, Sutherland GR (1993) Incidence and origin of “null” alleles in the (AC)n microsatellite markers. Am J Hum Gen 52:922–927

    PubMed  CAS  Google Scholar 

  • Chakraborty R, de Andrade M, Daiger SP, Budowle B (1992) Apparent heterozygote deficiencies observed in DNA typing data and their implications in forensic applications. Ann Hum Gen 56:45–57

    Article  CAS  Google Scholar 

  • Crozier RH, Kaufmann B, Carew ME, Crozier YC (1999) Mutability of microsatellites developed for the ant Camponotus consobrinus. Mol Ecol 8:271–276

    Article  PubMed  CAS  Google Scholar 

  • Dai CF, Fan TY, Yu JK (2000) Reproductive isolation and genetic differentiation of a scleractinian coral, Mycedium elephantosus. Mar Ecol Prog Ser 201:179–187

    Article  Google Scholar 

  • Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci 91:3166–3170

    Article  PubMed  CAS  Google Scholar 

  • Duran S, Pascual M, Estoup A, Turon X (2004) Strong population structure in the marine sponge Crambe crambe (Poecilosclerida) as revealed by microsatellite markers. Mol Ecol 13:511–522

    Article  PubMed  CAS  Google Scholar 

  • Gaggiotti OE, Lange O, Rassmann K, Gliddons C (1999) A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data. Mol Ecol 8:1513–1520

    Article  PubMed  CAS  Google Scholar 

  • Gilmour JP (2002) Substantial asexual recruitment of mushroom corals contributes little to population genetics of adults in conditions of chronic sedimentation. Mar Ecol Prog Ser 25:81–91

    Article  Google Scholar 

  • Goodman SJ (1997) R ST calc: a collection of computer programs for calculating estimates of genetic differentiation from microsatellite data and a determining of their significance. Mol Ecol 6:881–885

    Article  CAS  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices Version 2.9.3. Available from http://www.unil.ch/izea/softwares/fstat.html [updated from Goudet (1995)]

  • Gutiérrez-Rodríguez C, Lasker HR (2004) Microsatellite variation reveals high levels of genetic variability and population structure in the gorgonian coral Pseudopterogorgia elisabethae across the Bahamas. Mol Ecol 13:2211–2221

    Article  PubMed  CAS  Google Scholar 

  • Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Ecosystems of the world 25: Coral reefs. Elsevier, New York, pp 133–207

    Google Scholar 

  • Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318

    Article  Google Scholar 

  • Hellberg ME (1994) Relationships between inferred levels of gene flow and geographic distance in a philopatric coral, Balanophyllia elegans. Evolution 48:1829–1854

    Article  Google Scholar 

  • Hellberg ME (1995) Stepping stone gene flow in the solitary coral Balanophyllia elegans: equilibrium and non-equilibrium at different spatial scales. Mar Biol 123:573–581

    Article  Google Scholar 

  • Hellberg ME (1996) Dependence of gene flow on geographic distance in two solitary corals with different larval dispersal capabilities. Evolution 50:1167–1175

    Article  Google Scholar 

  • Hoffman RJ (1986) Variation in contributions of asexual reproduction to the genetic structure of populations of the sea anemone Metridium senile. Evolution 40:357–365

    Article  Google Scholar 

  • Hohenlohe PA (2004) Limits to gene flow in marine animals with planktonic larvae: models of Littorina species around point conception, California. Biol J Linn Soc 82:169–187

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Kalinowski ST (2005) Do polymorphic markers need large sample sizes to estimate genetic distances? Heredity 94:33–36

    Article  PubMed  CAS  Google Scholar 

  • Kayser M, Roewer L, Hedman M et al. (2000) Characteristics and frequency of germline mutations at microsatellite loci from the human Y chromosome, as revealed by direct observation in father/son pairs. Am J Hum Gen 66:1580–1588

    Article  PubMed  CAS  Google Scholar 

  • Launey S, Ledu C, Boudry P, Bonhomme F, Naciri-Graven Y (2002) Geographic structure in the European flat oyster (Ostrea edulis L.) as revealed by microsatellite polymorphism. J Hered 93:331–338

    Article  PubMed  CAS  Google Scholar 

  • Le Goff-Vitry MC, Pybus OG, Rogers AD (2004) Genetic structure of the deep-sea coral Lophelia pertusa in the northeast Atlantic revealed by microsatellites and internal transcribed spacers. Mol Ecol 13:537–549

    Article  PubMed  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 

  • Mantel N (1967) The detection of desease clustering and a generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • McFadden CS (1997) Contributions of sexual and asexual reproduction to population structure in the clonal soft coral, Alcyonium rudyi. Evolution 51:112–126

    Article  Google Scholar 

  • Miller KJ (1997) Genetic structure of black coral populations in New Zealand’s fjords. Mar Ecol Prog Ser 161:123–132

    Article  Google Scholar 

  • Miller KJ (1998) Short-distance dispersal of black coral larvae: inference from spatial analysis of colony genotypes. Mar Ecol Prog Ser 163:225–233

    Article  Google Scholar 

  • Miller K, Mundy C (2003) Rapid settlement in broadcast spawning corals: implications for larval dispersal. Coral Reefs 22:99–106

    Article  Google Scholar 

  • Nishikawa A, Katoh M, Sakai K (2003) Larval settlement rates and gene flow of broadcast-spawning (Acropora tenuis) and planula-brooding (Stylophora pistillata) corals. Mar Ecol Prog Ser 256:87–97

    Article  CAS  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 

  • Pemberton JM, Slate J, Bancroft DR, Barrett JA (1995) Non-amplifying alleles at microsatellite loci: a caution for parentage and population studies. Mol Ecol 4:249–252

    PubMed  CAS  Google Scholar 

  • Perez-Losada M, Guerra A, Carvalho GR, Sanjuan A, Shaw PW (2002) Extensive population subdivision of the cuttlefish Sepia officinalis (Mollusca: Cephalopoda) around the Iberian Peninsula indicated by microsatellite DNA variation. Heredity 89:417–424

    Article  PubMed  CAS  Google Scholar 

  • Perrin C, Wing SR, Roy MS (2004) Effects of hydrographic barriers on population genetic structure of the sea star Coscinasterias muricata (Echinodermata, Asteroidea) in the New Zealand fjords. Mol Ecol 13:2183–2195

    Article  PubMed  CAS  Google Scholar 

  • Petersen D, Tollrian R (2001) Methods to enhance sexual recruitment for restoration of damaged reefs. Bull Mar Sci 69:989–1000

    Google Scholar 

  • Reichow D, Smith MJ (2001) Microsatellites reveal high levels of gene flow among populations of the California squid Loligo opalescens. Mol Ecol 10:1101–1109

    Article  PubMed  CAS  Google Scholar 

  • Richmond RH (1987) Energetics, competency, and long-distance dispersal of planula larvae of the coral Pocillopora damicornis. Mar Biol 93:527–533

    Article  Google Scholar 

  • Ridgway T, Hoegh-Guldberg O, Ayre DJ (2001) Panmixia in Pocillopora verrucosa from South Africa. Mar Biol 139:175–181

    Article  CAS  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    PubMed  CAS  Google Scholar 

  • Russo CAM, Solé-Cava AM, Thorpe JP (1994) Population structure and genetic variation in two tropical sea anemones (Cnidaria, Actinidae) with different reproductive strategies. Mar Biol 119:267–276

    Article  Google Scholar 

  • Sammarco PW (1982) Polyp bail-out: an escape response to environmental stress and a new means of reproduction in corals. Mar Ecol Prog Ser 10:57–65

    Article  Google Scholar 

  • Skold M, Wing SR, Mladenov PV (2003) Genetic subdivision of a sea star with high dispersal capability in relation to physical barriers in a fjordic seascape. Mar Ecol Prog Ser 250:163–174

    Article  CAS  Google Scholar 

  • Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279

    Article  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    PubMed  CAS  Google Scholar 

  • Stoddart JA (1984a) Genetical structure within populations of the coral Pocillopora damicornis. Mar Biol 81:19–30

    Article  CAS  Google Scholar 

  • Stoddart JA (1984b) Genetic differentiation amongst populations of the coral Pocillopora damicornis off Southwestern Australia. Coral Reefs 3:149–156

    Article  Google Scholar 

  • Stoddart JA, Taylor JF (1988) Genotypic diversity: estimation and prediction in samples. Genetics 118:705–711

    PubMed  CAS  Google Scholar 

  • Veron JEN (2000) Corals of the World, vol 2, Australian Institute of Marine Science, Townsville

  • Viard F, Franck P, Dubois MP, Estoup A, Jarne P (1998) Variation of microsatellite size homoplasy across electromorphs, loci, and populations in three invertebrate species. J Mol Evol 47:42–51

    Article  PubMed  CAS  Google Scholar 

  • Wahlund S (1928) Zusammensetzung von Populationen und Korrelationserscheinungen vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas 11:65–106

    Article  Google Scholar 

  • Waples RS (1987) A multispecies approach to the analysis of gene flow in marine shore fishes. Evolution 41:385–400

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: F st ≠ 1/(4 Nm+1). Heredity 82:117–125

    Article  PubMed  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    PubMed  CAS  Google Scholar 

  • Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395–420

    Article  Google Scholar 

  • Wright S (1969) The evolution and genetics of populations, vol 2. The theory of gene frequencies. University of Chicago Press, Chicago, IL

  • Yu JK, Wang HY, Lee SC, Dai CF (1999) Genetic structure of a scleractinian coral, Mycedium elephantosus, in Taiwan. Mar Biol 133:21–28

    Article  Google Scholar 

  • Yund PO, McCartney MA (1994) Male reproductive success in sessile invertebrates: competition for fertilizations. Ecology 75:2151–2167

    Article  Google Scholar 

Download references

Acknowledgements

The Egyptian Environmental Affairs Agency and the Israel Nature and Parks Authority kindly gave us permission to sample S. hystrix from the Red Sea. This study was funded by the Minerva Foundation, the Minerva Center for Marine Invertebrates Immunology and Developmental Biology and by a grant from the Deutsche Forschungsgemeinschaft (NU 51/5 to BN and RT). We thank all people who provided field assistance, especially M. Rehberg and L. Bongiorni. We are grateful to X. Turon for running the simulations to evaluate the possible occurrence of clonal reproduction. We also thank J.M. Bohn for his help with the figures and A. Baird for carefully checking our English.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elke Maier.

Additional information

Communicated by O. Kinne, Oldendorf/Luhe

Appendix

Appendix

For a given population and locus with n apparent homozygotes, we computed the likelihood of all possible genotype sets in which 1, 2,... n homozygotes had been replaced by heterozygotes involving a null allele. Non-amplifying colony/locus combinations were interpreted as null homozygotes provided that the other two loci of the same colony had amplified, thus controlling for poor DNA quality. The likelihood computations were based on allele frequency estimates from the modified genotype sets under the assumption of random mating. The alternate data set was assembled from the maximum-likelihood genotype sets per population and locus. The estimated maximal local frequencies of null alleles that were inferred by our method were 0.21 (Sh4.24), 0.25 (Sh2.15) and 0.37 (Sh3.32). The minimal local estimates were zero for all three loci. Whenever our method detected the presence of a null allele in a given locus/site combination (ML frequency > 0), its frequency correlated very strongly (r>0.75) with estimates from two published methods (Chakraborty et al. 1992; Brookfield 1996). These approaches compute null allele frequencies solely based on observed heterozygote deficits, either with (Brookfield 1996) or without (Chakraborty et al. 1992) including non-amplifying samples as data (= null homozygotes). It is interesting to note, though, that there were cases in which our ML frequency of the null allele was zero, while the F IS-based methods inferred appreciable non-zero frequencies. In all of these cases, the likelihood curve was rather flat so that no particular estimate was strongly supported. It appears that the consideration of the specific genotypic constellations by our method (rather than just F IS) tended to favour the hypothesis of no null allele in these cases. In keeping with these observations, F IS estimates based on the alternate data set were not necessarily zero but they were non-significant throughout.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maier, E., Tollrian, R., Rinkevich, B. et al. Isolation by distance in the scleractinian coral Seriatopora hystrix from the Red Sea. Marine Biology 147, 1109–1120 (2005). https://doi.org/10.1007/s00227-005-0013-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-005-0013-6

Keywords

Navigation