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Contrasting population genetic structures of sympatric, mass-spawning Caribbean corals

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Abstract

Coral reef conservation management policy often focuses on larval retention and recruitment of marine fish with scant data available on important, less motile reef-building species such as corals. To evaluate the concept of population connectivity in corals, we tested whether broadcast spawning reproduction per se confers the same degree of dispersal to two sister species, Montastraea annularis (Anthozoa: Scleractinia; Ellis and Solander 1786) and M. faveolata (Ellis and Solander 1786), both dominant taxa in reefs of the northern Caribbean. Genetic analyses of ten nuclear DNA loci (seven microsatellite and three single-copy RFLP) reveal strikingly different patterns of population genetic subdivision for these closely related, sympatric species, in spite of likely identical dispersal abilities. Strong population genetic structure typified the architecture of M. annularis, whereas M. faveolata populations were principally genetically well mixed. A higher level of clonality was observed in M. annularis potentially because of a susceptibility to physical fragmentation. Clonality did not, however, significantly contribute to population genetic structure or low-level Hardy–Weinberg and linkage disequilibria observed in some populations. The lack of consistent association between reproductive mode and dispersal reinforces the perspective that population connectivity is not so much a function of predictable marine population source and sink relationships as is due to a more complex interface of oceanic currents interacting with and amplifying stochastic fluctuations in larval supply and settlement success. Our results support others promoting an overall ecosystem approach in marine protected area design.

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References

  • 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

    Article  CAS  Google Scholar 

  • Ayre DJ, Hughes TP (2004) Climate change, genotypic diversity and gene flow in reef-building corals. Ecol Lett 7:273–278

    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  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bode M, Bode L, Armsworth PR (2006) Larval dispersal reveals regional sources and sinks in the Great Barrier Reef. Mar Ecol Prog Ser 308:17–25

    Article  Google Scholar 

  • Budd AE, Pandolfi JM (2004) Overlapping species boundaries and hybridization within the Montastraeaannularis” reef coral complex in the Pleistocene of the Bahama Islands. Paleobiol 30:396–425

    Article  Google Scholar 

  • Cattell MV, Karl SA (2004) Genetics and morphology in a Borrichia frutescens and B. arborescens (Asteraceae) hybrid zone. Am J Bot 91:1757–1766

    Article  CAS  Google Scholar 

  • Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis models and estimation procedures. Evolution 3:550–557

    Article  Google Scholar 

  • Cho LL, Woodley JD (2002) Recovery of coral reef at Discovery Bay, Jamaica and the role of Diadema antillarum. Proc Nin Intl Coral Reef Symp 1:331–338

    Google Scholar 

  • Coffroth MA, Lasker HR (1998) Population structure of a clonal gorgonian coral: the interplay between clonal reproduction and disturbance. Evolution 52:379–393

    Article  Google Scholar 

  • Connell JH, Hughes TP, Wallace CC (1997) A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecol Mon 67:461–488

    Article  Google Scholar 

  • Cowen RK, Luiza KM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287:857–859

    Article  CAS  Google Scholar 

  • Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527

    Article  CAS  Google Scholar 

  • Criales MM, Lee TN (1995) Larval distribution and transport of penaeoid shrimps during the presence of the Tortugas Gyre in May-June, 1991. Fish Bull USA 93:471–482

    Google Scholar 

  • Edmunds PJ (1994) Evidence that reef-wide patterns of coral bleaching may be the result of the distribution of bleaching-susceptible clones. Mar Biol 121:137–142

    Article  Google Scholar 

  • Edmunds PJ, Carpenter RC (2001) Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef. Proc Natl Acad Soc USA 98:5067–5071

    Article  CAS  Google Scholar 

  • Ellis J, Solander D (1786) The natural history of many curious and uncommon zoophytes. Benjamin White and Son, London, p 208 63 pls

  • Fukami H, Budd AF, Levitan DR et al (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  Google Scholar 

  • Gardner TA, Cote IM, Gil JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960

    Article  CAS  Google Scholar 

  • Goldstein DB, Linares AR, Cavalli-Sforza LL, Feldman MW (1995) Genetic absolute dating based on microsatellites and the origin of modern humans. Proc Natl Acad Sci USA 92:6723–6727

    Article  CAS  Google Scholar 

  • Gomez A, Carvalho GR (2000) Sex, parthenogenesis and genetic structure of rotifers: microsatellite analysis of contemporary and nesting egg bank populations. Mol Ecol 9:203–214

    Article  CAS  Google Scholar 

  • Goodman SF (1997) RSTCALC: a collection of computer programs for calculating unbiased estimates of genetic differentiation and gene flow from microsatellite data and determining their significance. Mol Ecol 6:881–885

    Article  CAS  Google Scholar 

  • Gregory JW (1895) Contributions to the paleontology and physical geology of the West Indies. Q J Geol Soc Lond 51:255–312

    Article  Google Scholar 

  • Gyory J, Mariano AJ, Ryan EH (2005) The Caribbean current ocean surface currents. http://www.oceancurrents.rsmas.miami.edu/caribbean/caribbean_2.html

  • Hamm DE, Burton RS (2000) Population genetics of black abalone, Haliotis cracherodii, along the central California coast. J Expl Mar Biol Ecol 254:235–247

    Article  CAS  Google Scholar 

  • Hedgecock D (1986) Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates? Bull Mar Sci 39:550–564

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

    Article  Google Scholar 

  • Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean reef. Science 265:1547–1551

    Article  CAS  Google Scholar 

  • Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR et al (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  CAS  Google Scholar 

  • Jones GP, Milicich MJ, Emslie MJ, Lunow C (1999) Self-recruitment in a coral reef fish population. Nature 402:802–804

    Article  CAS  Google Scholar 

  • Jones GP, McCormick MI, Srinivasan M, Eagle JV (2004) Coral decline threatens fish biodiversity in marine reserves. Pro Natl Acad Sci USA 101:8251–8253

    Article  CAS  Google Scholar 

  • Karl SA, Avise JC (1992) Balancing selection at allozyme loci in oysters: implications from nuclear RFLPs. Science 256:100–102

    Article  CAS  Google Scholar 

  • Karl SA, Bowen BW, Avise JC (1992) Global populations structure and male-mediated gene flow in the green turtle (Chelonia mydas): RFLP analyses of anonymous nuclear DNA regions. Genetics 131:163–173

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kleypas JA, Buddemeier RW, Archer D et al (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118–120

    Article  CAS  Google Scholar 

  • Knowlton N (2001) The future of coral reefs. Proc Natl Acad Sci USA 98:5419–5425

    Article  CAS  Google Scholar 

  • Knowlton N, Jackson JBC (1993) Inbreeding and outbreeding in marine invertebrates. In: Thornhill NW (ed) The natural history of inbreeding and outbreeding. University of Chicago Press, Chicago, pp 200–249

    Google Scholar 

  • Knowlton N, Weil E, Weigt LA, Guzman HM (1992) Sibling species in Montastraea annularis, coral bleaching, and the coral climate record. Science 255:330–33

    Article  CAS  Google Scholar 

  • Knowlton N, Mate JL, Guzman HM, Rowan R, Jara J (1997) Direct evidence for reproductive isolation among the three species of the Montastraea annularis complex in Central America (Panama and Honduras). Mar Biol 127:705–711

    Article  Google Scholar 

  • Kramarsky-Winter E, Fine M, Loya Y (1997) Coral polyp expulsion. Nature 387:137

    Article  CAS  Google Scholar 

  • Lee TN, Williams E (1999) Mean distribution and seasonal variability of coastal currents and temperature in the Florida Keys with implications for larval recruitment. Bull Mar Sci 64:35–56

    Google Scholar 

  • Lee TN, Rooth C, Williams E et al (1992) Influence of Florida Current, gyres and wind-driven circulation on transport of larvae and recruitment in the Florida Keys coral reefs. Cont Shelf Res 12:971–1002

    Article  Google Scholar 

  • Lee TN, Clarke ME, Williams E, Szmant AF, Berger T (1994) Evolution of the Tortugas gyre and its influence on recruitment in the Florida Keys. Bull Mar Sci 54:621–646

    Google Scholar 

  • Leis JM (2002) Pacific coral-reef fishes: the implications of behavior and ecology of larvae for biodiversity and conservation, and a reassessment of the open population paradigm. Enviro Biol Fish 65:199–208

    Article  Google Scholar 

  • Levitan DR, Fukami H, Jara J et al (2004) Mechanisms of reproductive isolation among sympatric broadcast-spawning corals of the Montastraea annularis species complex. Evolution 58:308–323

    Article  Google Scholar 

  • Limouzy-Paris CB, Graber HC, Jones DL, Ropke AW, Richards WJ (1997) Translocation of larval coral reef fishes via sub-mesoscale spin-off eddies from the Florida current. Bull Mar Sci 60:966–983

    Google Scholar 

  • Mackenzie JB, Munday PL, Willis BL, Miller DJ, Van Oppen MJH (2004) Unexpected patterns of genetic structuring among locations but not color morphs in Acropora nasuta (Cnidaria; Scleractinia). Mol Ecol 13:9–20

    Article  CAS  Google Scholar 

  • Martin B, Nienhuis J, King G, Schaefer A (1989) Restriction fragment length polymorphisms associated with water use efficiency in tomato. Science 243:1725–1728

    Article  CAS  Google Scholar 

  • Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference to microsatellite loci. Genetics 142:1061–1064

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miller KJ, Ayre DJ (2004) The role of sexual and asexual reproduction in structuring high latitude populations of the reef coral Pocillopora damicornis. Heredity 92:557–568

    Article  CAS  Google Scholar 

  • Minch E (1995) Microsat Version 1.4. Stanford University, Stanford

  • Murphy SJ, Hurlburt HE (1999) The connectivity of eddy variability in the Caribbean Sea, the Gulf of Mexico, and the Atlantic Ocean. J Geophy Res 104:1431–1453

    Article  Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Article  Google Scholar 

  • Ogden JC (1997) Marine managers look upstream for connections. Science 278:1414–1415

    Article  CAS  Google Scholar 

  • Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Apps 13:S146–S158

    Article  Google Scholar 

  • Pandolfi JM, Lovelock CE, Budd AF (2002) Character release following extinction in a Caribbean reef coral species complex. Evolution 56:479–501

    Article  Google Scholar 

  • Pandolfi JM, Bradbury RH, Sala E et al (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958

    Article  CAS  Google Scholar 

  • Paterson A, Lander E, Hewitt J, Peterson S, Lincoln S, Tanksley S (1988) Resolution of quantitative traits into Mendelian factors by using a complete linkage map of restriction length polymorphisms. Nature 335:721–726

    Article  CAS  Google Scholar 

  • Reusch TBH, Stam WT, Olsen JL (2000) A microsatellite-based estimation of clonal diversity and population subdivision in Zostera marina, a marine flowering plant. Mol Ecol 9:127–140

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Roberts CM (1997) Connectivity and management of Caribbean coral reefs. Science 278:1454–1457

    Article  CAS  Google Scholar 

  • Roberts CM, Schmidt KF (1997) ‘No-take’ zones spark fisheries debate. Science 277:489–491

    Article  Google Scholar 

  • Rocha LA, Bass AL, Robertson DR, Bowen BW (2002) Adult habitat preferences, larval dispersal, and the comparative phylogeography of three Atlantic surgeonfishes (Teleostei: Acanthuridae). Mol Ecol 11:243–252

    Article  CAS  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  Google Scholar 

  • Rogers CS (1992) A matter of scale: damage from Hurricane Hugo (1989) to U.S. Virgin Islands reefs at the colony, community, and whole reef level. Proc Sev Intl Coral Reef Symp 1:127–133

    Google Scholar 

  • Rogers CS, McLain L, Tobias C (1991) Effects of Hurricane Hugo (1989) on a coral reef in St. John. Mar Ecol Proc Ser 78:189–199

    Article  Google Scholar 

  • Sammarco PW, Andrews JC (1988) Localized dispersal and recruitment in Great Barrier Reef corals: The Helix experiment. Science 239:1422–1424

    Article  CAS  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin version 2.000: A software for population genetics data analysis. Genetics and Biometry Laboratory - University of Geneva, Geneva

  • Severance EG, Szmant AM, Karl SA (2004a) Microsatellite loci isolated from the Caribbean coral, Montastraea annularis. Mol Ecol Notes 4:74–76

    Article  CAS  Google Scholar 

  • Severance EG, Szmant AM, Karl SA (2004b) Single-copy gene markers isolated from the Caribbean coral, Montastraea annularis. Mol Ecol Notes 4:167–169

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sokal RR, Rohlf JF (1995) Biometry. 3rd edn. WH Freeman, San Francisco

    Google Scholar 

  • Stenberg P, Lundmark M, Saura A (2003) MLGsim: a program for detecting clones using a simulation approach. Mol Ecol Notes 3:329–331

    Article  CAS  Google Scholar 

  • Sunnucks P, England PR, Taylor AC, Hales DF (1996) Microsatellite and chromosome evolution of parthenogenic Sitobio aphids in Australia. Genetics 144:747–756

    CAS  PubMed  PubMed Central  Google Scholar 

  • Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799–802

    Article  CAS  Google Scholar 

  • Szmant AM (1991) Sexual reproduction by the Caribbean reef corals Montastraea annularis and M. cavernosa. Mar Ecol Prog Ser 74:13–25

    Article  Google Scholar 

  • Szmant AM, Weil E, Miller MW, Colon DE (1997) Hybridization within the species complex of the Scleractinian coral Montastraea annularis. Mar Biol 129:561–572

    Article  Google Scholar 

  • Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109

    Article  CAS  Google Scholar 

  • Tunnicliffe V (1981) Breakage and propagation of the stony coral, Acropora cervcornis. Proc Natl Acad Sci USA 78:2427–2431

    Article  CAS  Google Scholar 

  • Van Veghel MLJ, Bak RPM (1993) Intraspecific variation of a dominant Caribbean reef building coral Montastraea annularis: genetic, behavioral and morphometric aspects. Mar Eco Prog Ser 92:255–265

    Article  Google Scholar 

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

  • Vollmer SV, Palumbi SR (2002) Hybridization and the evolution of reef coral diversity. Science 296:2023–2025

    Article  CAS  Google Scholar 

  • Walsh HE, Metzger DA, Higuchi R (1991) Chelex 100 medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10:506–513

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Wellington GM, Fitt WK (2003) Influence of UV radiation on the survival of larvae from broadcast-spawning reef corals. Mar Biol 143:1185–1192

    Article  CAS  Google Scholar 

  • Wolanski E (1994) Physical oceanographic processes of the Great Barrier Reef. CRC Press, Boca Raton

    Google Scholar 

  • Yeung C, McGowan MF (1991) Differences in inshore-offshore and vertical distribution of phyllosoma larvae of Panulirus, Scyllarus, and Sylloarides in the Florida Keys in May-June 1989. Bull Mar Sci 49:699–714

    Google Scholar 

  • Yeung C, Lee TN (2002) Larval transport and retention of the spiny lobster, Panulirus argus, in the coastal zone of the Florida Keys, USA. Fish Ocean 11:286–309

    Article  Google Scholar 

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Acknowledgements

We thank D. Hagman and E. Weil for providing samples from Mexico and Puerto Rico, respectively; A. Bass, C. Curtis, J. Garey, M. Garvey, K. Hayes, C. Lund, K. Overholtzer, L. Robbins, T. Schwartz and the staff at the Florida Keys National Marine Sanctuary for help in obtaining samples; A. Szmant for generously providing gamete bundles used for the genomic library construction; I Baums, B. Bowen, M. Craig, N. Knowlton, C. Puchulutegui, L. Rocha, A. Szmant, M. Zacks and anonymous reviewers for comments on this and previous drafts. Financial support for this work was provided by the Fred and Helen Tharp Foundation and Florida Sea Grant/Aylesworth Foundation grants to E.G.S. and by Florida Institute of Oceanography and National Science Foundation Grant in Systematics DEB 98-06905 to SAK.

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Correspondence to Stephen A. Karl.

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Communicated by S. Nishida, Tokyo

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Severance, E.G., Karl, S.A. Contrasting population genetic structures of sympatric, mass-spawning Caribbean corals. Mar Biol 150, 57–68 (2006). https://doi.org/10.1007/s00227-006-0332-2

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