Advertisement

Geographic distances and ocean currents influence Caribbean Acropora palmata population connectivity in the Lesser Antilles

  • Aurélien Japaud
  • Claude Bouchon
  • Hélène Magalon
  • Cécile FauvelotEmail author
Research Article
  • 76 Downloads

Abstract

The critically endangered coral species Acropora palmata used to dominate shallow Caribbean reefs but since the early 1980s, populations have dramatically declined. At the Caribbean scale, A. palmata is divided into two genetically divergent lineages and most of previous works investigating population connectivity among populations involved the western lineage (in Florida, the Bahamas, the Mesoamerican Reef System, and the Greater Antilles). Small scale genetic connectivity among A. palmata populations was globally found, possibly enhancing populations’ recovery at the local scale. Yet, little is known regarding the genetic connectivity of populations of the eastern lineage, especially those of the Lesser Antilles, a fragmented archipelago located at the edge of the species distribution. Here, we filled this gap by investigating the genetic diversity, population structure and connectivity of A. palmata populations among 36 sampled sites from 11 islands of the Lesser Antilles using 14 hypervariable microsatellite loci. Globally, genetic diversity levels in A. palmata populations from the Lesser Antilles were lower compared to what was previously reported within the Wider Caribbean. The analysis of the genetic structure, crossed with spatial autocorrelation analysis, revealed an isolation-by-distance pattern at both reef and Lesser Antilles scales. A gene dispersal distance of less than a kilometer, and a northward gene flow direction, in agreement with ocean surface currents in the region were found. Altogether, our results suggest a restricted population connectivity and short distance dispersal of A. palmata larvae within the Lesser Antilles further limited by geographic distances among suitable habitat patches. Additionally, our results suggest that southernmost populations are potential sources of larvae for the most northerly islands and have a key role in reseeding A. palmata populations of the Lesser Antilles.

Keywords

Acropora Lesser Antilles Larval dispersal, connectivity Genetic diversity Isolation-by-distance 

Notes

Acknowledgements

We thank Sébastien Cordonnier, Jean-Loup Manceau, Julien Lequellec, Didier Laplace and Emmanuel Badias for assistance on the field. We further thank the staff of the “Parc National de la Guadeloupe”, the “Réserve Naturelle des îlots de Petite-Terre”, the “Réserve Naturelle Nationale de Saint Barthélemy”, the “Réserve Naturelle Nationale de Saint-Martin”, the crew of the RV ANTEA during PACOTILLES campaign ( https://doi.org/10.17600/15005200), Christophe Menkès for providing the ocean current map and Simon Van Wynsberge for geographic distance estimations with barriers. We sincerely thank two anonymous reviewers for their valuable comments and suggestions on previous versions of the manuscript. This project was co-funded by the Laboratoire d’Excellence CORAIL (Agence nationale de la recherche, France) and the Agence des Aires Marine Protégées (France).

Supplementary material

10592_2019_1145_MOESM1_ESM.pdf (625 kb)
Supplementary material 1 (PDF 625 KB)
10592_2019_1145_MOESM2_ESM.pdf (877 kb)
Supplementary material 2 (PDF 876 KB)
10592_2019_1145_MOESM3_ESM.pdf (970 kb)
Supplementary material 3 (PDF 970 KB)
10592_2019_1145_MOESM4_ESM.pdf (640 kb)
Supplementary material 4 (PDF 639 KB)
10592_2019_1145_MOESM5_ESM.pdf (758 kb)
Supplementary material 5 (PDF 757 KB)
10592_2019_1145_MOESM6_ESM.pdf (626 kb)
Supplementary material 6 (PDF 625 KB)
10592_2019_1145_MOESM7_ESM.pdf (736 kb)
Supplementary material 7 (PDF 735 KB)

References

  1. Acropora Biological Review Team (2005) Atlantic Acropora Status ReviewGoogle Scholar
  2. Aguilar-Perera A, Hernández-Landa RC (2017) Occurrence of large thickets of Acropora prolifera (Scleractinia: Acroporidae) in the southern Gulf of Mexico. Mar Biodivers 48:2203–2205  https://doi.org/10.1007/s12526-017-0685-4 CrossRefGoogle Scholar
  3. Andras JP, Rypien KL, Harvell CD (2013) Range-wide population genetic structure of the Caribbean sea fan coral, Gorgonia ventalina. Mol Ecol 22:56–73.  https://doi.org/10.1111/mec.12104 CrossRefGoogle Scholar
  4. Aronson RB, Bruckner AW, Moore JA et al (2008) Acropora cervicornis. IUCN Red List Threat Species e.T133381A3716457Google Scholar
  5. 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.  https://doi.org/10.1111/j.0014-3820.2000.tb00704.x CrossRefGoogle Scholar
  6. Bak RPM (1975) Ecological aspects of the distribution of reef corals in the Netherlands Antilles. Bijdr Tot Dierkd 45:181–190Google Scholar
  7. Baums IB (2008) A restoration genetics guide for coral reef conservation. Mol Ecol 17:2796–2811.  https://doi.org/10.1111/j.1365-294X.2008.03787.x CrossRefGoogle Scholar
  8. Baums IB, Hughes CR, Hellberg ME (2005a) Mendelian microsatellite loci for the Caribbean coral Acropora palmata. Mar Ecol Prog Ser 288:115–127.  https://doi.org/10.3354/meps288115 CrossRefGoogle Scholar
  9. Baums IB, Miller MW, Hellberg ME (2005b) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390.  https://doi.org/10.1111/j.1365-294X.2005.02489.x CrossRefGoogle Scholar
  10. Baums IB, Miller MW, Hellberg ME (2006a) Geographic variation in clonal structure in a reef-building Caribbean coral, Acropora palmata. Ecol Monogr 76:503–519CrossRefGoogle Scholar
  11. Baums IB, Paris CB, Chérubin LM (2006b) A bio-oceanographic filter to larval dispersal in a reef-building coral. Limnol Oceanogr 51:1969–1981CrossRefGoogle Scholar
  12. Baums IB, Devlin-Durante MK, Brown L, Pinzón JH (2009) Nine novel, polymorphic microsatellite markers for the study of threatened Caribbean acroporid corals. Mol Ecol Resour 9:1152–1158.  https://doi.org/10.1111/j.1755-0998.2009.02588.x CrossRefGoogle Scholar
  13. Beaumont MA, Zhang W, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035Google Scholar
  14. Belkhir K, Borsa P, Chikhi L et al (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Lab Génome Popul Interact CNRS UMR 5000 Univ Montp II Montp FrGoogle Scholar
  15. Bouchon C, Portillo P, Bouchon-Navaro Y et al (2008) Status of coral reefs of the Lesser Antilles: the French West Indies, The Netherlands Antilles, Anguilla, Antigua, Grenada, Trinidad and Tobago. In: Status of coral reefs of the World: 2008. Australian Institute of Marine Science, Townsville, pp 265–280Google Scholar
  16. Bruckner AW (2002) Proceedings of the Caribbean Acropora Workshop: potential application of the U.S. endangered species act as a conservation strategy, In: Proceedings of the Caribbean Acropora Workshop. p 199Google Scholar
  17. Carpenter KE, Abrar M, Aeby GS et al (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563 (Supplementary Material)CrossRefGoogle Scholar
  18. Chamberland VF, Vermeij MJA, Brittsan M et al (2015) Restoration of critically endangered elkhorn coral (Acropora palmata) populations using larvae reared from wild-caught gametes. Glob Ecol Conserv 4:526–537.  https://doi.org/10.1016/j.gecco.2015.10.005 CrossRefGoogle Scholar
  19. Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631.  https://doi.org/10.1093/molbev/msl191 CrossRefGoogle Scholar
  20. Coffroth MA, Lasker HR (1998) Population structure of a clonal gorgonian coral: the interplay between clonal reproduction and disturbance. Evolution 52:379–393CrossRefGoogle Scholar
  21. Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527.  https://doi.org/10.1126/science.1122039 CrossRefGoogle Scholar
  22. Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc B 39:1–38Google Scholar
  23. Devlin-Durante MK, Baums IB (2017) Genome-wide survey of single-nucleotide polymorphisms reveals fine-scale population structure and signs of selection in the threatened Caribbean elkhorn coral, Acropora palmata. PeerJ 5:e4077.  https://doi.org/10.7717/peerj.4077 CrossRefGoogle Scholar
  24. Drury C, Paris CB, Kourafalou VH, Lirman D (2018) Dispersal capacity and genetic relatedness in Acropora cervicornis on the Florida Reef Tract. Coral Reefs 37:585–596.  https://doi.org/10.1007/s00338-018-1683-0 CrossRefGoogle Scholar
  25. Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361.  https://doi.org/10.1007/s12686-011-9548-7 CrossRefGoogle Scholar
  26. 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.  https://doi.org/10.1111/j.1365-294X.2005.02553.x CrossRefGoogle Scholar
  27. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567.  https://doi.org/10.1111/j.1755-0998.2010.02847.x CrossRefGoogle Scholar
  28. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491Google Scholar
  29. Faircloth BC (2006) GMCONVERT: file conversion for GENEMAPPER output files. Mol Ecol Notes 6:968–970.  https://doi.org/10.1111/j.1471-8286.2006.01419.x CrossRefGoogle Scholar
  30. Fogarty ND (2010) Reproductive isolation and hybridization dynamics in threatened Caribbean Acroporid corals. Nova Southeastern UniversityGoogle Scholar
  31. Fogarty ND (2012) Caribbean acroporid coral hybrids are viable across life history stages. Mar Ecol Prog Ser 446:145–159.  https://doi.org/10.3354/meps09469 CrossRefGoogle Scholar
  32. Fogarty ND, Vollmer SV, Levitan DR (2012) Weak prezygotic isolating mechanisms in threatened Caribbean Acropora corals. PLoS ONE 7:e30486.  https://doi.org/10.1371/journal.pone.0030486 CrossRefGoogle Scholar
  33. Francisco-Ortega J, Santiago-Valentín E, Acevedo-Rodríguez P et al (2007) Seed plant genera endemic to the Caribbean Island biodiversity hotspot: a review and a molecular phylogenetic perspective. Bot Rev 73:183–234.  https://doi.org/10.1663/0006-8101(2007)73%5B183:SPGETT%5D2.0.CO;2 CrossRefGoogle Scholar
  34. Fukami H, Omori M, Shimoike K et al (2003) Ecological and genetic aspects of reproductive isolation by different spawning times in Acropora corals. Mar Biol 142:679–684.  https://doi.org/10.1007/s00227-002-1001-8 CrossRefGoogle Scholar
  35. Galindo HM, Olson DB, Palumbi SR (2006) Seascape genetics: a coupled oceanographic-genetic model predicts population structure of Caribbean corals. Curr Biol 16:1622–1626.  https://doi.org/10.1016/j.cub.2006.06.052 CrossRefGoogle Scholar
  36. Garcia Reyes J, Schizas N (2010) No two reefs are created equal: fine-scale population structure in the threatened coral species Acropora palmata and A. cervicornis. Aquat Biol 10:69–83.  https://doi.org/10.3354/ab00254 CrossRefGoogle Scholar
  37. Goreau TF (1959) The ecology of Jamaican coral reefs I. Species composition and zonation. Ecology 40:67–90.  https://doi.org/10.2307/1929924 CrossRefGoogle Scholar
  38. Hardy OJ, Vekemans X (1999) Isolation by distance in a continuous population: reconciliation between spatial autocorrelation analysis and population genetics models. Heredity 83:145–154CrossRefGoogle Scholar
  39. Hardy OJ, Vekemans X (2002) SPAGEDI: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620.  https://doi.org/10.1046/j.1471-8278 CrossRefGoogle Scholar
  40. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Ecosystems of the world—coral reefs. Elsevier, Amsterdam, pp 133–207Google Scholar
  41. Hayashibara T, Shimoike K, Kimura T et al (1993) Patterns of coral spawning at Akajima Island, Japan. Mar Ecol Prog Ser 101:253–262CrossRefGoogle Scholar
  42. Heck KL, McCoy ED (1978) Long-distance dispersal and the reef-building corals of the Eastern Pacific. Mar Biol 48:349–356CrossRefGoogle Scholar
  43. Hedges SB, Díaz LM (2011) The Conservation Status Of Amphibians in The West Indies. In: Wilson BS, Hailey A, Horrocks JA (eds) Conservation of Caribbean Island Herpetofaunas Volume 1: Conservation Biology and the Wider Caribbean. Brill, Leiden, pp 31–48CrossRefGoogle Scholar
  44. Hellberg ME (2007) Footprints on water: the genetic wake of dispersal among reefs. Coral Reefs 26:463–473.  https://doi.org/10.1007/s00338-007-0205-2 CrossRefGoogle Scholar
  45. Hemond EM, Vollmer SV (2010) Genetic diversity and connectivity in the threatened staghorn coral (Acropora cervicornis) in Florida. PLoS ONE 5:e8652.  https://doi.org/10.1371/journal.pone.0008652 CrossRefGoogle Scholar
  46. Highsmith RC (1982) Reproduction by fragmentation in corals. Mar Ecol Prog Ser 7:207–226.  https://doi.org/10.3354/meps007207 CrossRefGoogle Scholar
  47. Hoffman JI, Grant SM, Forcada J, Phillips CD (2011) Bayesian inference of a historical bottleneck in a heavily exploited marine mammal. Mol Ecol 20:3989–4008.  https://doi.org/10.1111/j.1365-294X.2011.05248.x CrossRefGoogle Scholar
  48. Hughes AR, Inouye BD, Johnson MTJ et al (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623.  https://doi.org/10.1111/j.1461-0248.2008.01179.x CrossRefGoogle Scholar
  49. 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.  https://doi.org/10.1093/bioinformatics/btm233 CrossRefGoogle Scholar
  50. Japaud A, Fauvelot C, Bouchon C (2014) Unexpected high densities of the hybrid coral Acropora prolifera (Lamarck 1816) in Guadeloupe Island, Lesser Antilles. Coral Reefs 33:593–593.  https://doi.org/10.1007/s00338-014-1169-7 CrossRefGoogle Scholar
  51. Japaud A, Bouchon C, Manceau JL, Fauvelot C (2015) High clonality in Acropora palmata and Acropora cervicornis populations of Guadeloupe, French Lesser Antilles. Mar Freshw Res 66:847.  https://doi.org/10.1071/mf14181 CrossRefGoogle Scholar
  52. Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026.  https://doi.org/10.1111/j.1365-294X.2008.03887.x CrossRefGoogle Scholar
  53. Knowlton N (2001) The future of coral reefs. Proc Natl Acad Sci USA 98:5419–5425.  https://doi.org/10.1073/pnas.091092998 CrossRefGoogle Scholar
  54. Latta SC (2012) Avian research in the Caribbean: past contributions and current priorities. J Field Ornithol 83:107–121.  https://doi.org/10.1111/j.1557-9263.2012.00361.x CrossRefGoogle Scholar
  55. Lirman D (2000) Fragmentation in the branching coral Acropora palmata (Lamarck): growth, survivorship, and reproduction of colonies and fragments. J Exp Mar Biol Ecol 251:41–57CrossRefGoogle Scholar
  56. Lirman D, Schopmeyer S, Galvan V et al (2014) Growth dynamics of the threatened Caribbean Staghorn Coral Acropora cervicornis: influence of host genotype, symbiont identity, colony size, and environmental setting. PLoS ONE 9:e107253.  https://doi.org/10.1371/journal.pone.0107253 CrossRefGoogle Scholar
  57. Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425.  https://doi.org/10.1002/j.1537-2197.1995.tb12679.x CrossRefGoogle Scholar
  58. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220Google Scholar
  59. Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge, 797 ppCrossRefGoogle Scholar
  60. Mège P, Schizas NV, Garcia Reyes J, Hrbek T (2015) Genetic seascape of the threatened Caribbean elkhorn coral, Acropora palmata, on the Puerto Rico shelf. Mar Ecol 36:195–209.  https://doi.org/10.1111/maec.12135 CrossRefGoogle Scholar
  61. 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.  https://doi.org/10.1038/sj.hdy.6800459 CrossRefGoogle Scholar
  62. Miller DJ, van Oppen MJH (2003) A “fair go” for coral hybridization. Mol Ecol 12:805–807CrossRefGoogle Scholar
  63. Miller WJ, Muller EM, Rogers CS et al (2009) Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the US Virgin Islands. Coral Reefs 28:925–937.  https://doi.org/10.1007/s00338-009-0531-7 CrossRefGoogle Scholar
  64. Miller MW, Williams DE, Fisch J (2016) Genet-specific spawning patterns in Acropora palmata. Coral Reefs.  https://doi.org/10.1007/s00338-016-1472-6 Google Scholar
  65. Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:146–158  https://doi.org/10.1890/10510761(2003)013%5B0146:PGDCAT%5D2.0.CO;2 CrossRefGoogle Scholar
  66. Peakall R, Smouse PE (2006) GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295.  https://doi.org/10.1111/j.1471-8286.2005.01155.x CrossRefGoogle Scholar
  67. Peakall R, Smouse PE (2012) GenALEx 6.5: genetic analysis in excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539.  https://doi.org/10.1093/bioinformatics/bts460 CrossRefGoogle Scholar
  68. Porto-Hannes I, Zubillaga AL, Shearer TL et al (2015) Population structure of the corals Orbicella faveolata and Acropora palmata in the Mesoamerican barrier reef system with comparisons over Caribbean basin-wide spatial scale. Mar Biol 162:81–98.  https://doi.org/10.1007/s00227-014-2560-1 CrossRefGoogle Scholar
  69. Postaire B, Gélin P, Bruggemann JH, Magalon H (2017) One species for one island? unexpected diversity and weak connectivity in a widely distributed tropical hydrozoan. Heredity 1–10.  https://doi.org/10.1038/hdy.2016.126
  70. Precht WF, Bruckner AW, Aronson RB, Bruckner RJ (2002) Endangered acroporid corals of the Caribbean. Coral Reefs 21:41–42CrossRefGoogle Scholar
  71. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959Google Scholar
  72. Quinn NJ, Kojis BL (2005) Patterns of sexual recruitment of acroporid coral populations on the West fore reef at discovery Bay, Jamaica. Rev Biol Trop 53:83–90Google Scholar
  73. R Core Team (2016) R: a language and environment for statistical computing. R Found Stat Comput Vienna Austria. ISBN 3-900051-07-0 https://www.R-Proj.org/
  74. Raymond M, Rousset F (1995) GENEPOP (Version 1.2): Population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  75. Reusch TBH, Ehlers A, Hämmerli A, Worm B (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc Natl Acad Sci USA 102:2826–2831.  https://doi.org/10.1073/pnas.0500008102 CrossRefGoogle Scholar
  76. Ritson-Williams R, Paul VJ, Arnold SN, Steneck RS (2010) Larval settlement preferences and post-settlement survival of the threatened Caribbean corals Acropora palmata and A. cervicornis. Coral Reefs 29:71–81.  https://doi.org/10.1007/s00338-009-0555-z CrossRefGoogle Scholar
  77. Rossetto M, Gross CL, Jones R, Hunter J (2004) The impact of clonality on an endangered tree (Elaeocarpus williamsianus) in a fragmented rainforest. Biol Conserv 117:33–39.  https://doi.org/10.1016/S0006-3207(03)00260-X CrossRefGoogle Scholar
  78. Rousset (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62.  https://doi.org/10.1046/j.1420-9101.2000.00137.x CrossRefGoogle Scholar
  79. Spalding MD, Fox HE, Allen GR et al (2007) Marine Ecoregions of the World: a Bioregionalization of Coastal and shelf areas. Bioscience 57:573–583CrossRefGoogle Scholar
  80. Stoddart JA, Taylor JF (1988) Genotypic diversity: estimation and prediction in samples. Genetics 118:705–711Google Scholar
  81. Sundqvist L, Keenan K, Zackrisson M et al (2016) Directional genetic differentiation and relative migration. Ecol Evol 6:3461–3475.  https://doi.org/10.1002/ece3.2096 CrossRefGoogle Scholar
  82. Szmant AM (1986) Reproductive ecology of Caribbean reef corals. Coral Reefs 5:43–53.  https://doi.org/10.1007/BF00302170 CrossRefGoogle Scholar
  83. Vallejo-Marín M, Dorken ME, Barrett SCH (2010) The ecological and evolutionary consequences of clonality for plant mating. Annu Rev Ecol Evol Syst 41:193–213.  https://doi.org/10.1146/annurev.ecolsys.110308.120258 CrossRefGoogle Scholar
  84. van Etten J (2015) Package ‘gdistance’, pp. 1–30Google Scholar
  85. van Oppen MJH, Willis BL, van Vugt HWJA, Miller DJ (2000) Examination of species boundaries in the Acropora cervicornis group (Scleractinia, Cnidaria) using nuclear DNA sequence analyses. Mol Ecol 9:1363–1373CrossRefGoogle Scholar
  86. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538.  https://doi.org/10.1111/j.1471-8286.2004.00684.x CrossRefGoogle Scholar
  87. van Loon EE, Cleary DFR, Fauvelot C (2007) ARES: software to compare allelic richness between uneven samples. Mol Ecol Notes 7:579–582.  https://doi.org/10.1111/j.1471-8286.2007.01705.x CrossRefGoogle Scholar
  88. Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935.  https://doi.org/10.1046/j.1365-294X.2004.02076.x CrossRefGoogle Scholar
  89. Veron JEN (1995) Corals in space and time. The biogeography and evolution of the Scleractinia. Cornell Un, LondonGoogle Scholar
  90. Veron JEN (2000) Corals of the World, vol 1. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  91. Vollmer SV, Palumbi SR (2002) Hybridization and the evolution of reef coral diversity. Science 296:2023–2025.  https://doi.org/10.1126/science.1069524 CrossRefGoogle Scholar
  92. Vollmer SV, Palumbi SR (2007) Restricted gene flow in the Caribbean staghorn coral Acropora cervicornis: implications for the recovery of endangered reefs. J Hered 98:40–50.  https://doi.org/10.1093/jhered/esl057 CrossRefGoogle Scholar
  93. von der Heyden S, Beger M, Toonen RJ et al (2014) The application of genetics to marine management and conservation: examples from the Indo-Pacific. Bull Mar Sci 90:123–158.  https://doi.org/10.5343/bms.2012.1079 CrossRefGoogle Scholar
  94. Wallace CC (1999) Staghorn corals of the World: a revision of the coral genus Acropora (Scleractinia; Astrocoeniina; Acroporidae) worldwide, with emphasis on morphology, phylogeny and biogeography. CSIRO, CanberraGoogle Scholar
  95. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370Google Scholar
  96. Williams DE, Miller MW (2005) Coral disease outbreak: pattern, prevalence and transmission in Acropora cervicornis. Mar Ecol Prog Ser 301:119–128CrossRefGoogle Scholar
  97. Williams DE, Miller MW, Kramer KL (2008) Recruitment failure in florida keys Acropora palmata, a threatened Caribbean coral. Coral Reefs 27:697–705.  https://doi.org/10.1007/s00338-008-0386-3 CrossRefGoogle Scholar
  98. Willis BL, van Oppen MJH, Miller DJ et al (2006) The role of hybridization in the evolution of reef corals. Annu Rev Ecol Evol Syst 37:489–517.  https://doi.org/10.1146/annurev.ecolsys.37.091305.110136 CrossRefGoogle Scholar
  99. Wright S (1940) Breeding structure of populations in relation to speciation. Am Nat 74:232–248CrossRefGoogle Scholar
  100. Yeoh S-R, Dai C-F (2009) The production of sexual and asexual larvae within single broods of the scleractinian coral, Pocillopora damicornis. Mar Biol 157:351–359.  https://doi.org/10.1007/s00227-009-1322-y CrossRefGoogle Scholar
  101. Young CN, Schopmeyer SA, Lirman D (2012) A review of reef restoration and coral propagation using the threatened genus Acropora in the Caribbean and Western Atlantic. Bull Mar Sci 88:1075–1098.  https://doi.org/10.5343/bms.2011.1143 CrossRefGoogle Scholar
  102. Zubillaga AL, Márquez LM, Cróquer A, Bastidas C (2008) Ecological and genetic data indicate recovery of the endangered coral Acropora palmata in Los Roques, Southern Caribbean. Coral Reefs 27:63–72.  https://doi.org/10.1007/s00338-007-0291-1 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.UMR 7208 BOREA, Laboratoire d’excellence-CORAIL, Université des AntillesPointe-à-PitreGuadeloupe
  2. 2.UMR ENTROPIE (IRD, Université de La Réunion, CNRS), Laboratoire d’excellence-CORAIL, IRD de NouméaNouméa cedexNew Caledonia
  3. 3.UMR ENTROPIE (Université de La Réunion, IRD, CNRS), Laboratoire d’excellence-CORAIL, Faculté des Sciences et TechnologiesSt Denis Cedex 09, La RéunionFrance
  4. 4.Université Côte d’Azur, CNRS, FRE 3729 ECOMERSNiceFrance
  5. 5.Sorbonne Université, CNRSVillefranche-sur-MerFrance

Personalised recommendations