Coral Reefs

, Volume 34, Issue 1, pp 301–311 | Cite as

Genetic connectivity of the broadcast spawning reef coral Platygyra sinensis on impacted reefs, and the description of new microsatellite markers

  • Y. C. Tay
  • A. M. E. Noreen
  • Suharsono
  • L. M. Chou
  • P. A. Todd


As tropical coral reef habitats continue to be lost or degraded, understanding the genetic diversity and connectivity among populations is essential for making informed management decisions. This is particularly important in rapidly developing, land-scarce nations (such as Singapore) that require targeted conservation efforts. Sixty percentage of Singapore’s coral cover has been lost over the past five decades, and with further coastal reclamation underway, it is imperative to understand the effects of development on coral connectivity. In this study, we used seven microsatellite markers, of which six are newly described here, to investigate the genetic diversity and connectivity of the massive hard coral Platygyra sinensis at nine sites in Singapore and three in the nearby Indonesian island of Bintan. Our results show that P. sinensis currently retains large effective population sizes, high genetic diversity, as well as high connectivity among sites within each locality, which suggest that these populations have good potential for continued survival provided that there are no island-wide disturbances. However, the Singapore Strait appears to be a mild barrier to gene flow, which may lead to an increased reliance on self-seeding at either location. We suggest some directions for their management based on these potential population boundaries, which can help pave the path for marine conservation planning in Singapore.


Platygyra sinensis Genetic connectivity Microsatellites Singapore Coastal impacts Larval dispersal 



Permission to conduct research sampling in Indonesia was obtained through the Indonesian Institute of Sciences (LIPI) and the State Ministry of Research and Technology (RISTEK), under the research permit number 12/TKPIPA/FRP/SM/XII/2009. We thank S Lance and the Savannah Ecology Laboratory for the microsatellite library construction, members of the Marine Biology Laboratory for their assistance in the field, and the staff of the Banyan Tree Bintan Conservation Laboratory for their logistical support. We also thank VE Chhatre for his guidance on the use of several of the genetic softwares, D Huang and DP Araújo for their comments on early drafts of the manuscript, and CJ Starger for the insightful comments and suggestions to improve the manuscript. Special thanks to R Meier for his constructive advice, and allowing the free access to and use of his laboratory facilities for conducting the genetic work. This research was supported by a grant from the Technical Committee on the Coastal and Marine Environment of Singapore (Grant No. R-154-000-411-490). The first author would also like to acknowledge the World Future Foundation (WFF) for their support of this research by awarding her the WFF PhD Prize in Environmental and Sustainability Research.

Supplementary material

338_2014_1206_MOESM1_ESM.docx (9.8 mb)
Supplementary material 1 (DOCX 10021 kb)


  1. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a FST-outlier method. BMC Bioinformatics 9:323CrossRefPubMedCentralPubMedGoogle Scholar
  2. Atchison A, Sammarco PW, Brazeau DA (2008) Genetic connectivity in corals on the Flower Garden Banks and surrounding oil/gas platforms, Gulf of Mexico. J Exp Mar Biol Ecol 365:1–12CrossRefGoogle Scholar
  3. Babcock RC (1991) Comparative demography of three species of scleractinian corals using age- and size-dependent classifications. Ecol Monogr 61:225–244CrossRefGoogle Scholar
  4. Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390CrossRefPubMedGoogle Scholar
  5. Baums IB, Devlin-Durante MK, Polato NR, Xu D, Giri S, Altman NS, Ruiz D, Parkinson JE, Boulay JN (2013) Genotypic variation influences reproductive success and thermal stress tolerance in the reef building coral, Acropora palmata. Coral Reefs 32:703–717CrossRefGoogle Scholar
  6. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B Biol Sci 263:1619–1626CrossRefGoogle Scholar
  7. Beerli P (2009) How to use Migrate or why are Markov chain Monte Carlo programs difficult to use? In: Bertorelle G, Bruford MW, Hauffe HC, Rizzoli A, Vernesi C (eds) Population genetics for animal conservation, conservation biology series, vol 17. Cambridge University Press, Cambridge, pp 42–79Google Scholar
  8. Bird MI, Pang WC, Lambeck K (2006) The age and origin of the Straits of Singapore. Palaeogeogr Palaeoclimatol Palaeoecol 241:531–538CrossRefGoogle Scholar
  9. Brazeau DA, Sammarco PW, Atchison A (2011) Micro-scale genetic heterogeneity and structure in coral recruitment: fine-scale patchiness. Aquat Biol 12:55–67CrossRefGoogle Scholar
  10. Brownstein MJ, Carpten JD, Smith JR (1996) Modulation of non-templated nucleotide addition by Taq Polymerase: primer modifications that facilitate genotyping. BioTechniques 20:1004–1010PubMedGoogle Scholar
  11. Carlsson J (2008) Effects of microsatellite null alleles on assignment testing. J Hered 99:616–623CrossRefPubMedGoogle Scholar
  12. Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortés J, Delbeek JC, Devantier L, Edgar GJ, Edwards AJ, Fenner D, Guzmán HM, Hoeksema BW, Hodgson G, Johan O, Licuanan WY, Livingstone SR, Lovell ER, Moore JA, Obura DO, Ochavillo D, Polidoro BA, Precht WF, Quibilan MC, Reboton C, Richards ZT, Rogers AD, Sanciangco J, Sheppard A, Sheppard C, Smith J, Stuart S, Turak E, Veron JEN, Wallace C, Weil E, Wood E (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321(5888):560–563CrossRefPubMedGoogle Scholar
  13. Chakraborty R, Zhong Y, Jin L, Budowle B (1994) Nondetectability of restriction fragments and independence of DNA fragment sizes within and between loci in RFLP typing of DNA. Am J Hum Genet 55:391–401PubMedCentralPubMedGoogle Scholar
  14. Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631CrossRefPubMedGoogle Scholar
  15. Chou LM (2006) Marine habitats in one of the world’s busiest harbours. In: Wolanski E (ed) The environment in Asia Pacific harbours. Springer, Netherlands, pp 377–391CrossRefGoogle Scholar
  16. Chua T-E, Gorre IRL, Ross SA, Bernad SR, Gervacio B, Ebarvia MC (2000) The Malacca Straits. Mar Pollut Bull 41:160–178CrossRefGoogle Scholar
  17. Combosch DJ, Vollmer SV (2011) Population genetics of an ecosystem-defining reef coral Pocillopora damicornis in the Tropical Eastern Pacific. PLoS One 6:e21200CrossRefPubMedCentralPubMedGoogle Scholar
  18. Császár NBM, Ralph PJ, Frankham R, Berkelmans R, van Oppen MJH (2010) Estimating the potential for adaptation of corals to climate warming. PLoS One 5:e9751CrossRefPubMedCentralPubMedGoogle Scholar
  19. Darling JA, Bagley MJ, Roman J, Tepolt CK, Geller JB (2008) Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus. Mol Ecol 17:4992–5007CrossRefPubMedGoogle Scholar
  20. Dikou A, van Woesik R (2006) Survival under chronic stress from sediment load: spatial patterns of hard coral communities in the southern islands of Singapore. Mar Pollut Bull 52:1340–1354CrossRefPubMedGoogle Scholar
  21. Earl DA, VonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  22. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  23. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedCentralPubMedGoogle Scholar
  24. Fukami H, Budd AF, Levitan DR, Jara J, Kersanach R, Knowlton N (2004) Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 58:324–337CrossRefPubMedGoogle Scholar
  25. Glaubitz JC (2004) CONVERT: A user-friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Mol Ecol Notes 4:309–310CrossRefGoogle Scholar
  26. Goudet J (1995) FSTAT (Version 1.2): A computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  27. Guest JR, Baird AH, Goh BPL, Chou LM (2005) Seasonal reproduction in equatorial reef corals. Invertebr Reprod Dev 48:207–218CrossRefGoogle Scholar
  28. Guest JR, Baird AH, Maynard JA, Muttaqin E, Edwards AJ, Campbell SJ, Yewdall K, Affendi YA, Chou LM (2012) Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS One 7:e33353CrossRefPubMedCentralPubMedGoogle Scholar
  29. Hanebuth T, Stattegger K, Grootes PM (2000) Rapid flooding of the Sunda Shelf: A late-glacial sea-level record. Science 288(5468):1033–1035CrossRefPubMedGoogle Scholar
  30. Hauser L, Seamons TR, Dauer M, Naish KA, Quinn TP (2006) An empirical verification of population assignment methods by marking and parentage data: hatchery and wild steelhead (Oncorhynchus mykiss) in Forks Creek, Washington, USA. Mol Ecol 15:3157–3173CrossRefPubMedGoogle Scholar
  31. Hodgson G (1990) Sediment and the settlement of larvae of the reef coral Pocillopora damicornis. Coral Reefs 9:41–43CrossRefGoogle Scholar
  32. Huang D, Meier R, Todd PA, Chou LM (2008) Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. J Mol Evol 66(2):167–174CrossRefPubMedGoogle Scholar
  33. Huang D, Tun KPP, Chou LM, Todd PA (2009) An inventory of zooxanthellate scleractinian corals in Singapore, including 33 new records. Raffles Bull Zool 22:69–80Google Scholar
  34. 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 23:1801–1806CrossRefPubMedGoogle Scholar
  35. Keshavmurthy S, Hsu C-M, Kuo C-Y, Meng P-J, Wang J-T, Chen CA (2012) Symbiont communities and host genetic structure of the brain coral Platygyra verweyi, at the outlet of a nuclear power plant and adjacent areas. Mol Ecol 21:4393–4407CrossRefPubMedGoogle Scholar
  36. Kwok CK, Ang PO Jr (2013) Inhibition of larval swimming activity of the coral (Platygyra acuta) by interactive thermal and chemical stresses. Mar Pollut Bull 74:264–273CrossRefPubMedGoogle Scholar
  37. LaJeunesse TC, Smith R, Walther M, Pinzón J, Pettay DT, McGinley M, Aschaffenburg M, Medina-Rosas P, Cupul-Magaña AL, Pérez AL, Reyes-Bonilla H, Warner ME (2010) Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proc R Soc Lond B Biol Sci 277:2925–2934CrossRefGoogle Scholar
  38. Lance SL, Light JE, Jones KL, Hagen C, Hafner JC (2010) Isolation and characterization of 17 polymorphic microsatellite loci in the kangaroo mouse, genus Microdipodops (Rodentia: Heteromyidae). Conserv Genet Resour 2:139–141CrossRefGoogle Scholar
  39. Lechner A, Keckeis H, Schludermann E, Loisl F, Humphries P, Glas M, Tritthart M, Habersack H (2013) Shoreline configurations affect dispersal patterns of fish larvae in a large river. ICES J Mar Sci. doi: 10.1093/icesjms/fst139 Google Scholar
  40. Mangubhai S, Souter PB, Grahn M (2007) Phenotypic variation in the coral Platygyra daedalea in Kenya: morphometry and genetics. Mar Ecol Prog Ser 345:105–115CrossRefGoogle Scholar
  41. Márquez LM, Mackenzie JB, Takabayashi M, Smith CR, Chen CA (2000) Difficulties in obtaining microsatellites from acroporid corals. Proc 9th Int Coral Reef Symp 1:139–144Google Scholar
  42. Marshall DJ, Monro K, Bode M, Keough MJ, Swearer S (2010) Phenotype-environment mismatches reduce connectivity in the sea. Ecol Lett 13:128–140CrossRefPubMedGoogle Scholar
  43. Miller KJ, Howard CG (2004) Isolation of microsatellites from two species of scleractinian coral. Mol Ecol Notes 4:11–13CrossRefGoogle Scholar
  44. Miller KJ, Ayre DJ (2008) Population structure is not a simple function of reproductive mode and larval type: insights from tropical corals. J Anim Ecol 77:713–724CrossRefPubMedGoogle Scholar
  45. Nakajima Y, Nishikawa A, Iguchi A, Sakai K (2012) Regional genetic differentiation among northern high-latitude island populations of a broadcast-spawning coral. Coral Reefs 31:1125–1133CrossRefGoogle Scholar
  46. National Population and Talent Division, NPTD (2013) The population white paper: a sustainable population for a dynamic Singapore.
  47. Ng CSL, Chen D, Chou LM (2012) Hard coral assemblages on seawalls in Singapore. TMSI St John's Island 10th Anniversary Volume: Contributions to Marine Science pp 75–79Google Scholar
  48. Ng WC, Morton B (2003) Genetic structure of the scleractinian coral Platygyra sinensis in Hong Kong. Mar Biol 143:963–968CrossRefGoogle Scholar
  49. Nunes FLD, Norris RD, Knowlton N (2011) Long distance dispersal and connectivity in amphi-Atlantic corals at regional and basin scales. PLoS One 6:e22298CrossRefPubMedCentralPubMedGoogle Scholar
  50. Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:146–158CrossRefGoogle Scholar
  51. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  52. Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  53. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539CrossRefPubMedGoogle Scholar
  54. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959PubMedCentralPubMedGoogle Scholar
  55. Qu X, Meng Q (2011) The economic importance of the Straits of Malacca and Singapore: An extreme-scenario analysis. Transp Res Part E Logist Transp Rev 48:258–265CrossRefGoogle Scholar
  56. Rodriguez-Lanetty M, Hoegh-Guldberg O (2002) The phylogeography and connectivity of the latitudinally widespread scleractinian coral Plesiastrea versipora in the Western Pacific. Mol Ecol 11:1177–1189CrossRefPubMedGoogle Scholar
  57. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of populations structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  58. Ryman N, Palm S (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol Ecol Notes 6:600–602CrossRefGoogle Scholar
  59. Sargent TD, Jamrich M, Dawid IB (1986) Cell interactions and the control of gene activity during early development of Xenopus laevis. Dev Biol 114:238–246CrossRefPubMedGoogle Scholar
  60. Severance EG, Karl SA (2006) Contrasting population genetic structures of sympatric, mass-spawning Caribbean corals. Mar Biol 150:57–68CrossRefGoogle Scholar
  61. Shearer TL, van Oppen MJH, Romano SL, Wörheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487CrossRefPubMedGoogle Scholar
  62. Souter P, Grahn M (2008) Spatial genetic patterns in lagoonal, reef-slope and island populations of the coral Platygyra daedalea in Kenya and Tanzania. Coral Reefs 27:433–439CrossRefGoogle Scholar
  63. Tan HT, Chou LM, Yeo DCJ, Ng PKL (2010) Waste- and reclaimed land. In: Tan HT, Chou LM, Yeo DCJ, Ng PKL (eds) The natural heritage of Singapore, 3rd edn. Prentice Hall-Pearson Education South Asia Pte Ltd, Singapore, p 78Google Scholar
  64. Tay YC, Guest JR, Chou LM, Todd PA (2011) Vertical distribution and settlement competencies in broadcast spawning coral larvae: implications for dispersal models. J Exp Mar Biol Ecol 409:324–330CrossRefGoogle Scholar
  65. Tay YC, Todd PA, Rosshaug PS, Chou LM (2012) Simulating the transport of broadcast coral larvae among the Southern Islands of Singapore. Aquat Biol 15:283–297CrossRefGoogle Scholar
  66. Underwood JN, Smith LD, van Oppen MJH, Gilmour JP (2009) Ecologically relevant dispersal of corals on isolated reefs: implications for managing resilience. Ecol Appl 19:18–29CrossRefPubMedGoogle Scholar
  67. van Oppen MJH, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15:3863–3883CrossRefPubMedGoogle Scholar
  68. 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:e3401CrossRefPubMedCentralPubMedGoogle Scholar
  69. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191PubMedCentralPubMedGoogle Scholar
  70. Wooldridge SA (2014) Differential thermal bleaching susceptibilities amongst coral taxa: re-posing the role of the host. Coral Reefs 33:15–27CrossRefGoogle Scholar
  71. Yasuda N, Nagai S, Hamaguchi M, Okaji K, Gérard K, Nadaoka K (2009) Gene flow of Acanthaster planci (L.) in relation to ocean currents revealed by microsatellite analysis. Mol Ecol 18:1574–1590CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Y. C. Tay
    • 1
  • A. M. E. Noreen
    • 2
  • Suharsono
    • 3
  • L. M. Chou
    • 4
  • P. A. Todd
    • 5
  1. 1.Evolutionary Biology Laboratory, Department of Biological SciencesNational University of SingaporeSingaporeSingapore
  2. 2.Applied Plant Ecology Lab, Department of Biological SciencesNational University of SingaporeSingaporeSingapore
  3. 3.Research Center for OceanographyIndonesian Institute of Sciences (LIPI)JakartaIndonesia
  4. 4.Reef Ecology Laboratory, Department of Biological SciencesNational University of SingaporeSingaporeSingapore
  5. 5.Experimental Marine Ecology Laboratory, Department of Biological SciencesNational University of SingaporeSingaporeSingapore

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