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

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Abstract

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.

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References

  • 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 9:323

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 365:1–12

    Article  CAS  Google Scholar 

  • Babcock RC (1991) Comparative demography of three species of scleractinian corals using age- and size-dependent classifications. Ecol Monogr 61:225–244

    Article  Google Scholar 

  • Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390

    Article  CAS  PubMed  Google Scholar 

  • 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 32:703–717

    Article  Google Scholar 

  • Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B Biol Sci 263:1619–1626

    Article  Google Scholar 

  • 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 42–79

    Google Scholar 

  • Bird MI, Pang WC, Lambeck K (2006) The age and origin of the Straits of Singapore. Palaeogeogr Palaeoclimatol Palaeoecol 241:531–538

    Article  Google Scholar 

  • Brazeau DA, Sammarco PW, Atchison A (2011) Micro-scale genetic heterogeneity and structure in coral recruitment: fine-scale patchiness. Aquat Biol 12:55–67

    Article  Google Scholar 

  • Brownstein MJ, Carpten JD, Smith JR (1996) Modulation of non-templated nucleotide addition by Taq Polymerase: primer modifications that facilitate genotyping. BioTechniques 20:1004–1010

    CAS  PubMed  Google Scholar 

  • Carlsson J (2008) Effects of microsatellite null alleles on assignment testing. J Hered 99:616–623

    Article  CAS  PubMed  Google Scholar 

  • 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):560–563

    Article  CAS  PubMed  Google Scholar 

  • 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 55:391–401

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  CAS  PubMed  Google Scholar 

  • 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 377–391

    Chapter  Google Scholar 

  • Chua T-E, Gorre IRL, Ross SA, Bernad SR, Gervacio B, Ebarvia MC (2000) The Malacca Straits. Mar Pollut Bull 41:160–178

    Article  Google Scholar 

  • Combosch DJ, Vollmer SV (2011) Population genetics of an ecosystem-defining reef coral Pocillopora damicornis in the Tropical Eastern Pacific. PLoS One 6:e21200

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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:e9751

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 17:4992–5007

    Article  CAS  PubMed  Google Scholar 

  • 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 52:1340–1354

    Article  CAS  PubMed  Google Scholar 

  • Earl DA, VonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 58:324–337

    Article  CAS  PubMed  Google Scholar 

  • Glaubitz JC (2004) CONVERT: A user-friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Mol Ecol Notes 4:309–310

    Article  CAS  Google Scholar 

  • Goudet J (1995) FSTAT (Version 1.2): A computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Guest JR, Baird AH, Goh BPL, Chou LM (2005) Seasonal reproduction in equatorial reef corals. Invertebr Reprod Dev 48:207–218

    Article  Google Scholar 

  • 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:e33353

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hanebuth T, Stattegger K, Grootes PM (2000) Rapid flooding of the Sunda Shelf: A late-glacial sea-level record. Science 288(5468):1033–1035

    Article  CAS  PubMed  Google Scholar 

  • 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 15:3157–3173

    Article  CAS  PubMed  Google Scholar 

  • Hodgson G (1990) Sediment and the settlement of larvae of the reef coral Pocillopora damicornis. Coral Reefs 9:41–43

    Article  Google Scholar 

  • 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):167–174

    Article  CAS  PubMed  Google Scholar 

  • Huang D, Tun KPP, Chou LM, Todd PA (2009) An inventory of zooxanthellate scleractinian corals in Singapore, including 33 new records. Raffles Bull Zool 22:69–80

    CAS  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  CAS  PubMed  Google Scholar 

  • 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 21:4393–4407

    Article  PubMed  Google Scholar 

  • 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 74:264–273

    Article  CAS  PubMed  Google Scholar 

  • 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 277:2925–2934

    Article  Google Scholar 

  • 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 2:139–141

    Article  Google Scholar 

  • 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 

  • Mangubhai S, Souter PB, Grahn M (2007) Phenotypic variation in the coral Platygyra daedalea in Kenya: morphometry and genetics. Mar Ecol Prog Ser 345:105–115

    Article  CAS  Google Scholar 

  • Márquez LM, Mackenzie JB, Takabayashi M, Smith CR, Chen CA (2000) Difficulties in obtaining microsatellites from acroporid corals. Proc 9th Int Coral Reef Symp 1:139–144

    Google Scholar 

  • Marshall DJ, Monro K, Bode M, Keough MJ, Swearer S (2010) Phenotype-environment mismatches reduce connectivity in the sea. Ecol Lett 13:128–140

    Article  CAS  PubMed  Google Scholar 

  • Miller KJ, Howard CG (2004) Isolation of microsatellites from two species of scleractinian coral. Mol Ecol Notes 4:11–13

    Article  CAS  Google Scholar 

  • 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 77:713–724

    Article  PubMed  Google Scholar 

  • 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 31:1125–1133

    Article  Google Scholar 

  • National Population and Talent Division, NPTD (2013) The population white paper: a sustainable population for a dynamic Singapore. http://www.nptd.gov.sg/content/NPTD/news/_jcr_content/par_content/download_98/file.res/population-white-paper.pdf

  • 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 75–79

    Google Scholar 

  • Ng WC, Morton B (2003) Genetic structure of the scleractinian coral Platygyra sinensis in Hong Kong. Mar Biol 143:963–968

    Article  Google Scholar 

  • Nunes FLD, Norris RD, Knowlton N (2011) Long distance dispersal and connectivity in amphi-Atlantic corals at regional and basin scales. PLoS One 6:e22298

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:146–158

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • 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 90:502–503

    Article  Google Scholar 

  • 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 95:536–539

    Article  CAS  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 48:258–265

    Article  Google Scholar 

  • 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 11:1177–1189

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of populations structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Ryman N, Palm S (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol Ecol Notes 6:600–602

    Article  Google Scholar 

  • Sargent TD, Jamrich M, Dawid IB (1986) Cell interactions and the control of gene activity during early development of Xenopus laevis. Dev Biol 114:238–246

    Article  CAS  PubMed  Google Scholar 

  • Severance EG, Karl SA (2006) Contrasting population genetic structures of sympatric, mass-spawning Caribbean corals. Mar Biol 150:57–68

    Article  Google Scholar 

  • Shearer TL, van Oppen MJH, Romano SL, Wörheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487

    Article  CAS  PubMed  Google Scholar 

  • 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 27:433–439

    Article  Google Scholar 

  • 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 78

    Google Scholar 

  • 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 409:324–330

    Article  Google Scholar 

  • Tay YC, Todd PA, Rosshaug PS, Chou LM (2012) Simulating the transport of broadcast coral larvae among the Southern Islands of Singapore. Aquat Biol 15:283–297

    Article  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, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15:3863–3883

    Article  PubMed  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:e3401

    Article  PubMed Central  PubMed  Google Scholar 

  • Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed Central  PubMed  Google Scholar 

  • Wooldridge SA (2014) Differential thermal bleaching susceptibilities amongst coral taxa: re-posing the role of the host. Coral Reefs 33:15–27

    Article  Google Scholar 

  • 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 18:1574–1590

    Article  PubMed  Google Scholar 

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Acknowledgments

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.

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Authors and Affiliations

  1. Evolutionary Biology Laboratory, Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Block S1A, #05-16, Singapore, 117543, Singapore

    Y. C. Tay

  2. Applied Plant Ecology Lab, Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore, 117543, Singapore

    A. M. E. Noreen

  3. Research Center for Oceanography, Indonesian Institute of Sciences (LIPI), Jl. Pasir Putih I, Ancol Timur, Jakarta, Indonesia

    Suharsono

  4. Reef Ecology Laboratory, Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore, 117543, Singapore

    L. M. Chou

  5. Experimental Marine Ecology Laboratory, Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore, 117543, Singapore

    P. A. Todd

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Correspondence to Y. C. Tay.

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Tay, Y.C., Noreen, A.M.E., Suharsono et al. Genetic connectivity of the broadcast spawning reef coral Platygyra sinensis on impacted reefs, and the description of new microsatellite markers. Coral Reefs 34, 301–311 (2015). https://doi.org/10.1007/s00338-014-1206-6

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