Advertisement

Marine Biology

, Volume 162, Issue 1, pp 81–98 | Cite as

Population structure of the corals Orbicella faveolata and Acropora palmata in the Mesoamerican Barrier Reef System with comparisons over Caribbean basin-wide spatial scale

  • I. Porto-HannesEmail author
  • A. L. Zubillaga
  • T. L. Shearer
  • C. Bastidas
  • C. Salazar
  • M. A. Coffroth
  • A. M. Szmant
Original Paper

Abstract

Studies of genetic diversity and population genetic structure in marine organisms are relevant to understanding populations’ variability, and therefore their ability to withstand environmental perturbations, their potential for resistance to local extinction and their natural rate of recovery. Population structure and genetic diversity were assessed at a regional spatial scale (i.e., Mesoamerican Barrier Reef System, MBRS) in two major reef building coral species Orbicella (formerly Montastraea) faveolata and Acropora palmata, and at a larger spatial scale (i.e., Caribbean-wide; MBRS, Panama, Venezuela and Puerto Rico) for A. palmata only. The most significant findings were as follows: (1) high genetic diversity and low clonality were found for both species, which is expected for O. faveolata but not for A. palmata, (2) both species showed low-to-moderate, yet significant population structure among populations along the MBRS; in particular, O. faveolata and A. palmata from Ambergris (Belize) and O. faveolata from Calabash (Belize) and A. palmata from Puerto Morelos (Mexico) showed some genetic differentiation from the rest of the MBRS populations, and (3) A. palmata from MBRS, Panama, Puerto Rico and Venezuela were grouped into four subregions that could be considered as management units. A more spatially detailed sampling program and the inclusion of recruits will be necessary to get a comprehensive understanding of coral population structure and current gene flow patterns in these two species.

Keywords

Venezuela Population Genetic Structure Allelic Richness Coral Species Coral Population 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors are grateful to P. Sale for his significant support, T. Snell at Georgia Institute of Technology, E. Weil at the University of Puerto Rico Mayaguez and the Biology Department at Universidad de los Andes for the access to their laboratories. We thank J. Azueta (Belize Fisheries Department) for permission to collect coral samples, and E. García (University of Belize) and J. Gibson (Wildlife Conservation Society) for field assistance in Belize. Permission to collect coral samples and field assistance in Mexico was provided by C. Gutiérrez, M. C. García (CONANP), M. I. Millet (PNAC), D. G. Muñoz (PNAPM), R. M. Loretto (PNAPM). We are grateful for field assistance by J. Craig, the staff and crews of the Mexico and Belize Marine Parks, E. Irrizary in Puerto Rico, H. Guzmán and A. Cróquer in Panama and A. Humanes, M. Caputo, M. Barbosa, and J. Dávila in Venezuela. Lastly, we thank, I. Baums, C. Riginos, an anonymous reviewer and R. Foster for carefully reading our manuscript and for giving detailed comments that were helpful in improving the manuscript. Los Roques sampling was funded by Decanato de Estudios de Postgrado, Universidad Simón Bolívar, and Misión Ciencia (Ministerio del Poder Popular para el Ambiente). This research was funded by the World Bank-GEF Coral Reef Targeted Research program and NSF OCE-0424996 (MAC).

Supplementary material

227_2014_2560_MOESM1_ESM.pdf (11 kb)
Supplementary material 1 (PDF 11 kb)
227_2014_2560_MOESM2_ESM.pdf (700 kb)
Supplementary material 2 (PDF 699 kb)
227_2014_2560_MOESM3_ESM.pdf (967 kb)
Supplementary material 3 (PDF 966 kb)
227_2014_2560_MOESM4_ESM.pdf (15 kb)
Supplementary material 4 (PDF 14 kb)
227_2014_2560_MOESM5_ESM.pdf (48 kb)
Supplementary material 5 (PDF 48 kb)
227_2014_2560_MOESM6_ESM.pdf (557 kb)
Supplementary material 6 (PDF 556 kb)
227_2014_2560_MOESM7_ESM.pdf (36 kb)
Supplementary material 7 (PDF 36 kb)
227_2014_2560_MOESM8_ESM.pdf (463 kb)
Supplementary material 8 (PDF 462 kb)
227_2014_2560_MOESM9_ESM.pdf (333 kb)
Supplementary material 9 (PDF 333 kb)

References

  1. Adjeroud M, Guérécheau A, Vidal-Dupiol J, Flot J-F, Arnaud-Haond S, Bonhomme F (2014) Genetic diversity, clonality and connectivity in the scleractinian coral Pocillopora damicornis: a multi-scale analysis in an insular, fragmented reef system. Mar Biol 161(3):531–541Google Scholar
  2. Allendorf FW (1986) Genetic drift and loss of alleles versus heterozygosity. Zoo Biol 5(2):181–190Google Scholar
  3. Altizer S, Harvell D, Friedle E (2003) Rapid evolutionary dynamics and disease threats to biodiversity. Trends Ecol Evol 11:589–596Google Scholar
  4. Anderson CD, Epperson BK, Fortin MJ, Holderegger R, James PMA, Rosenberg MS, Scribner KT, Spears S (2010) Considering spatial and temporal scale in landscape-genetic studies of gene flow. Mol Ecol 19:3565–3575Google Scholar
  5. Andras JP, Rypien KL, Harvell CD (2013) Range-wide population genetic structure of the Caribbean Sea fan coral, Gorgonia ventalina. Mol Ecol 22(1):56–73Google Scholar
  6. Aronson RB, Precht WF (2001) White-band disease and the changing face of Caribbean coral reefs. Hydrobiologia 460:25–38Google Scholar
  7. Aronson RB, Precht WF, Macintyre IG, Murdoch TJT (2000) Coral bleach-out in Belize. Nature 405(6782):36Google Scholar
  8. Aronson RB, Bruckner A, Moore J, Precht B, Weil E (2008) Acropora palmata and Montastraea (Orbicella) faveolata IUCN 2014. IUCN red list of threatened species. Version 2014.1. http://www.iucnredlist.org. Accessed 07 July 2014
  9. Bak RP, Nieuwland G, Meesters EH (2005) Coral reef crisis in deep and shallow reefs: 30 years of constancy and change in reefs of Curacao and Bonaire. Coral Reefs 24:475–479Google Scholar
  10. Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11(2):155–165Google Scholar
  11. Banks SC, Piggott MP, Williamson JE, Bovè U, Holbrock NJ, Beheregaray LB (2007) Oceanic variability and coastal topography shape genetic structure in a long-dispersing sea urchin. Ecology 88:3055–3064Google Scholar
  12. Baums IB (2008) A restoration genetics guide for coral reef conservation. Mol Ecol 7:2796–2811Google Scholar
  13. Baums IB, Miller MW, Hellberg ME (2005a) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390Google Scholar
  14. Baums IB, Hughes CR, Hellberg ME (2005b) Mendelian microsatellite loci for the Caribbean coral Acropora palmata. Mar Ecol Prog Ser 288:115–127Google Scholar
  15. Baums IB, Miller MW, Hellberg ME (2006) Geographic variation in clonal structure in a reef-building Caribbean coral, Acropora palmata. Ecol Monogr 76:503–519Google Scholar
  16. Baums IB, Johnson ME, Devlin-Durante MK, Miller MW (2010) Host population genetic structure and zooxanthellae diversity of two reef-building coral species along the Florida Reef Tract and wider Caribbean. Coral Reefs 29:835–842Google Scholar
  17. 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 32:703–717Google Scholar
  18. Bellwood DR, Hughes TP, Folke C, Nystrom M (2004) Confronting the coral reef crisis. Nature 429:827–833Google Scholar
  19. Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs. Coral Reefs 29(2):309–327Google Scholar
  20. Bowen BW, Bass AL, Muss A, Carlin J, Robertson DR (2006) Phylogeography of two Atlantic squirrelfishes (family Holocentridae): exploring links between pelagic larval duration and population connectivity. Mar Biol 149:899–913Google Scholar
  21. Briggs JC (1974) Marine zoogeography. McGraw-Hill, New YorkGoogle Scholar
  22. Bruckner AW, Bruckner RJ (2006) Consequences of yellow band disease (YBD) on Montastraea annularis (species complex) populations on remote reefs off Mona Island, Puerto Rico. Dis Aquat Org 69:67–73Google Scholar
  23. Bruckner AW, Hill RL (2009) Ten years of change to coral communities off Mona and Desecheo Islands, Puerto Rico, from disease and bleaching. Dis Aquat Org 87:19–31Google Scholar
  24. Budd AF, Fukami H, Smith ND, Knowlton N (2012) Taxonomic classification of the reef coral family Mussidae (Cnidaria: Anthozoa: Scleractinia). Zool J Linn Soc 166:465–529Google Scholar
  25. Butler MJ IV, Paris CB, Goldstein JS, Matsuda H, Cowen RK (2011) Behavior constrains the dispersal of long-lived spiny lobster larvae. Mar Ecol Prog Ser 422:223–237Google Scholar
  26. Bythell JC, Sheppard CR (1993) Mass mortality of Caribbean shallow corals. Mar Poll Bull 26(6):296–297Google Scholar
  27. Carilli J, Norris RD, Black B, Walsh S, McField M (2009) Local stressors reduce coral resilience to bleaching. PLoS One 4:e6324Google Scholar
  28. Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631Google Scholar
  29. Charlesworth B (1998) Measures of divergence between populations and the effect of forces that reduce variability. Mol Biol Evol 15:538–543Google Scholar
  30. Chérubin LM, Kuchinke CP, Paris CB (2008) Ocean circulation and terrestrial runoff dynamics in the Mesoamerican region from spectral optimization of SeaWiFS data and a high resolution simulation. Coral Reefs 27(3):503–519Google Scholar
  31. Coffroth MA, Lasker HR (1998) Population structure of a clonal gorgonian coral: the interplay between clonal reproduction and disturbance. Evolution 52:379–393Google Scholar
  32. Coles SL, Brown BE (2003) Coral bleaching: capacity for acclimatization and adaptation. Adv Mar Biol 46:183–223Google Scholar
  33. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014Google Scholar
  34. Cortés J (ed) (2003) Latin American coral reefs. Elsevier Science B.V, AmsterdamGoogle Scholar
  35. Courchamp F, Clutton-Brock T, Grenfell B (1999) Inverse density dependence and the Allee effect. Trends Ecol Evol 14:405–410Google Scholar
  36. Cowen RK, Lwiza KM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287:857–859Google Scholar
  37. Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527Google Scholar
  38. Cróquer A, Weil A (2009) Changes in Caribbean coral disease prevalence after the 2005 bleaching event. Dis Aquat Org 87:33–43Google Scholar
  39. D’Croz L, Maté JL (2004) Experimental responses to elevated water temperature in genotypes of the reef coral Pocillopora damicornis from upwelling and non-upwelling environments in Panama. Coral Reefs 23:473–483Google Scholar
  40. Díaz-Ferguson E, Haney RA, Wares JP, Silliman BR (2010) Population genetics of a trochid gastropod broadens picture of Caribbean genetic connectivity. PLoS One 5:e12675Google Scholar
  41. DiBattista JD (2008) Patterns of genetic variation in anthropogenically impacted populations. Conserv Genet 9:141–156Google Scholar
  42. Duffy JE (1993) Genetic population structure in two tropical sponge dwelling shrimps that differ in dispersal potential. Mar Biol 116:459–470Google Scholar
  43. Earl DA, von Holdt BM (2012) Structure harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361Google Scholar
  44. Edmunds PJ, Elahi R (2007) The demographics of a 15-year decline in cover of the Caribbean reef coral Montastraea annularis. Ecol Monogr 77:3–18Google Scholar
  45. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620Google Scholar
  46. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587Google Scholar
  47. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null allele. Mol Ecol Notes 7:574–578Google Scholar
  48. Foster NL, Baums IB, Mumby PJ (2007) Sexual vs. asexual reproduction in an ecosystem engineer: the massive coral Montastraea annularis. J Anim Ecol 76:384–391Google Scholar
  49. Foster NL, Paris CB, Kool JT, Baums IB, Stevens JR, Sanchez JA, Bastidas C, Agudelo C, Bush P, Day O, Ferrari R, Gonzalez P, Gore S, Guppy R, McCartney MA, Coy CMC, Mendes J, Srinivasan A, Steiner S, Vermeij MJA, Weil E, Mumby PJ (2012) Connectivity of Caribbean coral populations: complementary insights from empirical and modeled gene flow. Mol Ecol 21:1143–1157Google Scholar
  50. Foster NL, Baums IB, Sanchez JA, Paris CB, Chollett I, Agudelo CL, Vermeij MJA, Mumby PJ (2013) Hurricane-driven patterns of clonality in an ecosystem engineer: the Caribbean coral Montastraea annularis. PLoS One 8(1):e53283Google Scholar
  51. Frankham R (2005) Genetics and extinction. Heredity 126:131–140Google Scholar
  52. Galindo HM, Olson DB, Palumbi SR (2006) Seascape genetics: a coupled oceanographic genetic model predicts population structure of Caribbean corals. Curr Biol 16:1622–1626Google Scholar
  53. Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960Google Scholar
  54. Garzón-Ferreira J, Gil-Aguledo DL, Barrios LM, Zea S (2001) Stony coral disease observed in southwestern Caribbean reefs. Hydrobiologia 460:65–69Google Scholar
  55. Gerlach G, Atema J, Kingsford MJ, Black KP, Miller-Sims V (2007) Smelling home can prevent dispersal of reef fish larvae. Proc Natl Acad Sci USA 104:858–863Google Scholar
  56. Gladfelter WB (1982) White-band disease in Acropora palmata-implications for the structure and growth of shallow reefs. Bull Mar Sci 32:639–643Google Scholar
  57. Gladfelter EH, Monahan RK, Gladfelter WB (1978) Growth rates of five reef-building corals in the northeastern Caribbean. Bull Mar Sci 28:728–734Google Scholar
  58. Goodbody-Gringley G, Woollacott RM, Giribet G (2011) Population structure and connectivity in the Atlantic scleractinian coral Montastraea cavernosa (Linnaeus, 1767). Mar Ecol 33:32–48Google Scholar
  59. Goodman SJ (1997) Rst Calc: a collection of computer programs for calculating estimates of genetic differentiation from microsatellite data and determining their significance. Mol Ecol 6:881–885Google Scholar
  60. Goudet J (1995) FSTAT version 1.2: a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  61. Goudet J (2002) FSTAT version 2.9.3.2. www2.unil.che/popgen/softwares/fstat.htm
  62. Gutiérrez-Rodríguez C, Lasker HR (2004) Reproductive biology, development, and planula behavior in the Caribbean gorgonian Pseudopterogorgia elisabethae. Invertebr Biol 123:54–67Google Scholar
  63. Haig SM (1998) Molecular contributions to conservation. Ecology 79:413–425Google Scholar
  64. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinski Z (ed) Ecosystems of the world, 25. Coral reefs. Elsevier, New York, pp 133–207Google Scholar
  65. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus ADME, Overstreet RM, Porter JW, Smith GW, Vasta GR (1999) Emerging marine diseases: climate links and anthropogenic factors. Science 285:1505–1510Google Scholar
  66. Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318Google Scholar
  67. Hepburn RI, Sale PF, Dixon B, Heath DD (2009) Genetic structure of juvenile cohorts of bicolour damselfish (Stegastes partitus) along the Mesoamerican barrier reef: chaos through time. Coral Reefs 28:277–288Google Scholar
  68. Highsmith RC (1982) Reproduction by fragmentation in corals. Mar Ecol Prog Ser 7:207–226Google Scholar
  69. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742Google Scholar
  70. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332Google Scholar
  71. Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551Google Scholar
  72. Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263Google Scholar
  73. Hughes TP, Baird AH, Dinsdale EA, Moltschaniwskyj NA, Pratchett MS, Tanner JE, Willis BL (2000) Supply-side ecology works both ways: the link between benthic adults, fecundity, and larval recruits. Ecology 81:2241–2249Google Scholar
  74. Hughes TP, Baird AH, Dinsdale EA, Harriott VJ, Moltschaniwskyj NA, Pratchett MS, Tanner JE, Willis BL (2002) Detecting regional variation using meta-analysis and large-scale sampling: latitudinal patterns in recruitment. Ecology 83:436–451Google Scholar
  75. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, PandolW JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637Google Scholar
  76. Jones GP, Almany GR, Russ GR, Sale PF (2009) Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28:307–325Google Scholar
  77. Knowlton N, Weil E, Weigt LA, Guzmán HM (1992) Sibling species in Montastraea annularis coral bleaching, and the coral climate record. Science 255:330–333Google Scholar
  78. Knowlton N, Maté JL, Guzmán HM, Rowan R, Jara J (1997) Direct evidence for reproductive isolation among of the Montastraea annularis complex in Central America (Panamá and Honduras). Mar Biol 127:705–711Google Scholar
  79. Kramer PA, Kramer PR (2002) In: McField (ed) Ecoregional conservation planning for the Mesoamerican Caribbean reef. World Wildlife Fund, Washington, DCGoogle Scholar
  80. Leberg PL (2002) Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol 11:2445–2449Google Scholar
  81. Lessios HA, Kessing BD, Robertson DR, Paulay G (1999) Phylogeography of the pantropical sea urchin Eucidaris in relation to land barriers and ocean currents. Evolution 53:806–817Google Scholar
  82. Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55:955–975Google Scholar
  83. Lessios HA, Kane J, Robertson DR (2003) Phylogeography of the pantropical sea urchin Tripneustes: contrasting patterns of population structure between oceans. Evolution 57:2026–2036Google Scholar
  84. Levin LA (2006) Recent progress in understanding larval dispersal: new directions and digressions. Int Comp Biol 46:282–297Google Scholar
  85. Lirman D (2000) Fragmentation in the branching coral Acropora palmata (Lamarck): growth, survivorship, and reproduction of colonies and fragments. J Exp Mar Biol Ecol 251:41–57Google Scholar
  86. Maynard JA, Anthony KRN, Marshall PA, Masiri I (2008) Major bleaching events can lead to increased thermal tolerance in corals. Mar Biol 155:173–182Google Scholar
  87. McFadden CS (1997) Contributions of sexual and asexual reproduction to population structure in the clonal soft coral, Alcyonium rudyi. Evolution 51:112–126Google Scholar
  88. McField M, Bood N, Fonseca A, Arrivillaga A, Franquesa Rinos A, Loreto Viruel RM (2008) Status of the Mesoamerican Reef after the 2005 coral bleaching event. In: Wilkinson C, Souter D (eds) Status of the Caribbean coral reefs after bleaching and hurricanes in 2005. Global Coral Reef Monitoring Network, and Reef and Rainforest Center, Townsville, pp 45–60Google Scholar
  89. Meirmans PG, Hedrick PW (2011) Assessing population structure: F ST and related measures. Mol Ecol Resour 11:5–18Google Scholar
  90. Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794Google Scholar
  91. Miller MW, Weil E, Szmant AM (2000) Coral recruitment and juvenile mortality as structuring factors for reef benthic communities in Biscayne National Park, USA. Coral Reefs 19:115–123Google Scholar
  92. Miller J, Waara R, Muller E, Rogers C (2006) Coral bleaching and disease combine to cause extensive mortality on corals reefs in US Virgin Islands. Coral Reefs 25:418Google Scholar
  93. Mitton JB, Berg CJ, Orr KS (1989) Population-structure, larval dispersal, and gene flow in the queen conch, Strombus gigas, of the Caribbean. Biol Bull 177:356–362Google Scholar
  94. Moritz C (1994) Defining ‘evolutionary significant units’ for conservation. Trends Ecol Evol 9:373–375Google Scholar
  95. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10Google Scholar
  96. Neigel JE, Avise JC (1983) Clonal diversity and population-structure in a reef building coral, Acropora cervicornis—self-recognition analysis and demographic interpretation. Evolution 37:437–453Google Scholar
  97. Nunes F, Norris RD, Knowlton N (2009) Implications of isolation and low genetic diversity in peripheral populations of an amphi-Atlantic coral. Mol Ecol 18:4283–4297Google Scholar
  98. Okubo N, Motokawa T, Omori M (2007) When fragmented coral spawn? Effect of size and timing on survivorship and fecundity of fragmentation in Acropora formosa. Mar Biol 151:353–363Google Scholar
  99. Ospina-Guerrero SP, Landinez-Garcia RM, Rodríguez-Castro DJ, Arango R, Marquez E (2008) Genetic connectivity of Stegastes partitus in the south Caribbean evidenced by microsatellite analysis. Cien Mar 34:155–163Google Scholar
  100. Paris C, Cherubin LM (2008) River-reef connectivity in the Meso-American region. Coral Reefs 27:773–781Google Scholar
  101. Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Australian National University, CanberraGoogle Scholar
  102. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539Google Scholar
  103. Pérez-Ruzafa A, González-Wangüemerta M, Lenfantb P, Marcosa C, García-Chartona JA (2006) Effects of fishing protection on the genetic structure of fish populations. Biol Conserv 129:244–255Google Scholar
  104. Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855Google Scholar
  105. Prada C, Hellberg M (2013) Long pre-reproductive selection and divergence by depth in a Caribbean candelabrum coral. Proc Nat Acad Sci USA 110:3961–3966Google Scholar
  106. Pritchard JK, Stephens M, Donelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959Google Scholar
  107. Pritchard JK, Wen X, Falush D (2010) Documentation for STRUCTURE software: version 2.3 http://pritchardlab.stanford.edu/structure_software/release_versions/v2.3.4/structure_doc.pdf. Accessed 17 Sept 2014
  108. Puebla O, Bermingham E, McMillan WO (2012) On the spatial scale of dispersal in coral reef fishes. Mol Ecol 21:5675–5688Google Scholar
  109. Purcell JFH, Cowen RK, Hughes CR, Williams DA (2006) Weak genetic structure indicates strong dispersal limits: a tale of two coral reef fish. Proc R Soc B 273:1483–1490Google Scholar
  110. Reed DH, Frankham R (2003) Population fitness is correlated with genetic diversity. Conserv Biol 17:230–237Google Scholar
  111. Restrepo JD, Kjerfve B (2000) Magdalena river: interannual variability (1975–1995) and revised water discharge and sediment load estimates. J Hydrol 235:137–149Google Scholar
  112. Roberts CM (1997) Connectivity and management of Caribbean coral reefs. Science 278:1454–1456Google Scholar
  113. Robertson DR, Green DG, Victor BC (1988) Temporal coupling of production and recruitment of larvae of a Caribbean reef Fish. Ecology 69:370–381Google Scholar
  114. Robins CR (1971) Distributional patterns of fishes from coastal and shelf waters of the tropical western Atlantic. FAO Fish Res 71:249–255Google Scholar
  115. Rocha LA, Bass AL, Robertson DR, Bowen BW (2002) Adult habitat preferences, larval dispersal, and the comparative phylogeography of three Atlantic surgeon-fishes (Teleostei: Acanthuridae). Mol Ecol 11:243–252Google Scholar
  116. Rodríguez-Martínez RE, Banaszak AT, McField MD, Beltrán-Torres AU, Álvarez-Filip L (2014) Assessment of Acropora palmata in the Mesoamerican Reef System. PLoS One 9(4):e96140Google Scholar
  117. Rogstad SH, Keane B, Beresh J (2002) Genetic variation across VNTR loci in central North American Taraxacum surveyed at different spatial scales. Plant Ecol 161:111–121Google Scholar
  118. Sala E, Molina-Urena H, Walter RP, Heath DD (2010) Local and regional genetic connectivity in a Caribbean coral reef fish. Mar Biol 157:437–445Google Scholar
  119. Sánchez JA, Alvarado EM, Gil M, Charry H, Arenas O, García Chasqui L, García Chasqui R (1999) Synchronous mass spawning of Montastraea annularis (Ellis & Solander) and Montastraea faveolata (Ellis & Solander) (Faviidae: Scleractinia) at Rosario Islands, Caribbean coast of Colombia. Bull Mar Sci 65(3):873–879Google Scholar
  120. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.0: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  121. Selkoe KA, Gaines SD, Caselle JE, Warner RR (2006) Current shifts and kin aggregation explain genetic patchiness in fish recruits. Ecology 87:3082–3094Google Scholar
  122. Severance EG, Karl SA (2006) Contrasting population genetic structures of sympatric, mass spawning Caribbean corals. Mar Biol 150:57–68Google Scholar
  123. Severance EG, Szmant AM, Karl SA (2004) Microsatellite loci isolated from the Caribbean coral, Montastraea annularis. Mol Ecol Notes 4:74–76Google Scholar
  124. Shanks AL (2009) Pelagic larval duration and dispersal distance revisited. Biol Bull 216(3):373–385Google Scholar
  125. Shanks AL, Grantham BA, Carr MH (2003) Propagule dispersal distance and the size and spacing of marine reserves. Ecol Appl 13:S159–S169Google Scholar
  126. Shearer TL, Porto I, Zubillaga AL, Coffroth MA (2009) Restoration of coral populations in light of genetic diversity. Coral Reefs 28(3):727–733Google Scholar
  127. Shulman MJ, Bermingham E (1995) Early life histories, ocean currents and the population genetics of Caribbean reef fishes. Evolution 49:1041–1061Google Scholar
  128. Smith SR (1992) Patterns of coral recruitment and post-settlement mortality on Bermuda’s reefs: comparisons to Caribbean and Pacific reefs. Am Zool 32:663–673Google Scholar
  129. Soto I, Andréfouët S, Hu C, Muller-Karger FE, Wall CC, Sheng J, Hatcher BG (2009) Physical connectivity in the Mesoamerican Barrier Reef System inferred from 9 years of ocean color observations. Coral Reefs 28:415–425Google Scholar
  130. Souter P, Henriksson O, Olsson N, Grahn M (2009) Patterns of genetic structuring in the coral Pocillopora damicornis on reefs in East Africa. BMC Ecol 9:19Google Scholar
  131. Sponaugle S, Cowen RK, Shanks A, Morgan SG, Leis JM, Pineda J, Boehlert GW, Kingsford MJ, Lindeman KC, Grimes C, Munro JL (2002) Predicting self-recruitment in marine populations: biophysical correlates and mechanisms. Bull Mar Sci 70(1):341–375Google Scholar
  132. Szmant AM, Weil M, Miller MW, Colon DE (1997) Hybridization within the species complex of the scleractinian coral Montastraea annularis (Ellis & Solander). Mar Biol 129:561–572Google Scholar
  133. Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109Google Scholar
  134. van Oppen MJH, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15:3863–3883Google Scholar
  135. Vermeij MJA, Fogarty ND, Miller MW (2006) Pelagic conditions affect larval behavior, survival and settlement patterns in the Caribbean coral Montastraea faveolata. Mar Ecol Prog Ser 310:119–128Google Scholar
  136. Villinski JT (2003) Depth-independent reproductive characteristics for the Caribbean reef-building coral Montastraea faveolata. Mar Biol 142:1043–1053Google Scholar
  137. Vollmer AV, Palumbi SR (2007) Restricted gene flow in the Caribbean staghorn coral Acropora cervicornis: implications for the recovery of endangered reefs. J Hered 98:40–50Google Scholar
  138. Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:438–450Google Scholar
  139. Weil E, Knowlton N (1994) A multi-character analysis of the Caribbean coral Montastraea annularis (Ellis and Solander 1786) and its two sibling species, M. faveolata (Ellis and Solander 1786) and M. franksi (Gregory 1895). Bull Mar Sci 55:151–175Google Scholar
  140. Weil E, Cróquer A, Urreiztieta I (2009) Yellow band disease compromises the reproductive output of the Caribbean reef-building coral Montastraea faveolata (Anthozoa, Scleractinia). Dis Aquat Org 87:45–55Google Scholar
  141. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38(6):1358–1370Google Scholar
  142. Wellington GM, Victor BC (1989) Planktonic larval duration of one hundred species of Pacific and Atlantic damselfishes (Pomacentridae). Mar Biol 101:557–567Google Scholar
  143. Wright S (1943) Isolation by distance. Genetics 28:114–138Google Scholar
  144. Wright S (1965) The interpretation of population structure by F-statistics with special regard to system of mating. Evolution 19:395–420Google Scholar
  145. Zakai D, Levy O, Chadwick-Furman NE (2000) Experimental fragmentation reduces sexual reproductive output by the reef-building coral Pocillopora damicornis. Coral Reefs 19:185–188Google Scholar
  146. Zubillaga AL (2010) El coral Acropora palmata: comportamiento, distribución larval y conectividad genética en el Caribe. Dissertation, Universidad Simon Bolivar, VenezuelaGoogle Scholar
  147. Zubillaga AL, Márquez LM, Cróquer A, Bastidas C (2008) Ecological and genetic data indicate recovery of endangered coral Acropora palmata in Los Roques, Southern Caribbean. Coral Reefs 27:63–72Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • I. Porto-Hannes
    • 1
    Email author
  • A. L. Zubillaga
    • 2
  • T. L. Shearer
    • 3
  • C. Bastidas
    • 2
  • C. Salazar
    • 4
  • M. A. Coffroth
    • 1
    • 5
  • A. M. Szmant
    • 6
  1. 1.Graduate Program in Evolution, Ecology and BehaviorState University of New York at BuffaloBuffaloUSA
  2. 2.Departamento de Biología de OrganismosUniversidad Simón BolívarCaracasVenezuela
  3. 3.School of BiologyGeorgia Institute of TechnologyAtlantaUSA
  4. 4.Programa de Biología, Facultad de Ciencias Naturales y MatemáticasUniversidad del RosarioBogotáColombia
  5. 5.Department of GeologyState University of New York at BuffaloBuffaloUSA
  6. 6.Center for Marine ScienceUniversity of North Carolina WilmingtonWilmingtonUSA

Personalised recommendations