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Marine Biology

, 163:165 | Cite as

Genetic diversity of reef fishes around Cuba: a multispecies assessment

  • Jessy Castellanos-GellEmail author
  • Aymée Robainas-Barcia
  • Fabián Pina-Amargós
  • Pedro Chevalier-Monteagudo
  • Cushla Metcalfe
  • Wagner Franco Molina
  • Didier Casane
  • Erik García-MachadoEmail author
Original paper

Abstract

We aimed to identify biotic and abiotic factors underlying genetic structure and diversity of reef fish around Cuba. For three species, Stegastes partitus, Haemulon flavolineatum and Acanthurus tractus, we investigated the effects of shared environmental factors, such as the geography of the Cuban Archipelago, and specific characteristics, such as life history traits, on genetic structure and diversity. Samples were collected at five locations around Cuba. For S. partitus and H. flavolineatum, mitochondrial DNA and microsatellite loci were examined, whereas only mitochondrial DNA polymorphism was analyzed for A. tractus. All three species showed high genetic diversity. Mismatch distribution analyses suggest past population expansion in all species, but at different times in each species. Haplotype network and population genetic analyses suggest that: (1) S. partitus went through a recent population bottleneck in the late Pleistocene, (2) H. flavolineatum went through a population bottleneck but earlier, in  the mid-Pleistocene, and (3) A. tractus has had a large and stable population size with coalescence times that go back to the late Pliocene. Genetic polymorphism in H. flavolineatum and A. tractus is homogeneous throughout the archipelago, whereas there is significant genetic structure in S. partitus. Genetic differentiation among S. partitus populations is most likely the result of the combined effects of egg type and oceanic current patterns along the Cuban coast.

Keywords

Genetic Differentiation Reef Fish Mismatch Distribution Larval Dispersal Coalescence Time 
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

We would like to thank Oscar Valmaña and Luis Sánchez for essential support with field work, and Gaspar González Sansón and Consuelo Aguilar Betancourt for valuable discussions on the ecology of marine fish. We also acknowledge Roamsy Volta for assistance with figure production. We thank also the three reviewers and the editor for their valuable comments and suggestions. This study was partially financed by the Research Grant A4139-1 from the International Foundation for Science awarded to ARB and the Embassy of France in Cuba.

Supplementary material

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References

  1. Alvarado-Bremer JR, Baker AJ, Mejuto J (1995) Mitochondrial DNA control region sequences indicate extensive mixing of swordfish (Xiphias gladius) populations in the Atlantic Ocean. Can J Fish Aquat Sci 52:1720–1732. doi: 10.1139/f95-764 CrossRefGoogle Scholar
  2. Amos W, Hoffman JI, Frodsham A, Zhang L, Best S, Hill AVS (2007) Automated binning of microsatellite alleles: problems and solutions. Mol Ecol Notes 7:10–14. doi: 10.1111/j.1471-8286.2006.01560.x CrossRefGoogle Scholar
  3. Arriaza L, Hernández M, Lorenzo S, Olivera J, Rodas L, Montesino D, Carrillo Y, Almeida I, Simanca J, Padrón JN (2012) Modelación numérica de corrientes marinas alrededor del occidente de Cuba. Ser Ocenol 10:11–22Google Scholar
  4. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  5. Bandelt H-J, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefGoogle Scholar
  6. Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390. doi: 10.1111/j.1365-294X.2005.02489.x CrossRefGoogle Scholar
  7. Bellwood DR, Wainwright PC (2002) The history and biogeography of fishes on coral reefs. In: Sale PF (ed) Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic Press, San Diego, pp 5–32CrossRefGoogle Scholar
  8. Bernardi G, Lape J (2005) Tempo and mode of speciation in the Baja California disjunct fish species Anisotremus davidsonii. Mol Ecol 14:4085–4096. doi: 10.1111/j.1365-294X.2005.02729.x CrossRefGoogle Scholar
  9. Bintanja R, van de Wal RSW (2008) North American ice-sheet dynamics and the onset of 100,000-year glacial cycles. Nature 454:869–872. http://www.nature.com/nature/journal/v454/n7206/suppinfo/nature07158_S1.html
  10. Bintanja R, van de Wal RSW, Oerlemans J (2005) Modelled atmospheric temperatures and global sea levels over the past million years. Nature 437:125–128. doi: 10.1038/nature03975 CrossRefGoogle Scholar
  11. Borrell Y, Espinosa G, Romo J, Vázquez E, Sánchez JA, Blanco G (2004) DNA microsatellites variability and genetic differentiation among natural populations of the Cuban white shrimp Litopenaeus schmitti. Mar Biol 144:327–333CrossRefGoogle Scholar
  12. 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 149:899–913CrossRefGoogle Scholar
  13. Bowen BW, Rocha LA, Toonen RJ, Karl SA, Laboratory T (2013) The origins of tropical marine biodiversity. TREE 28:359–366. doi: 10.1016/j.tree.2013.01.018 Google Scholar
  14. Bradbury IR, Laurel B, Snelgrove PVR, Bentzen P, Campana SE (2008) Global patterns in marine dispersal estimates: the influence of geography, taxonomic category and life history. Proc R Soc B 275:1803–1809. doi: 10.1098/rspb.2008.0216 CrossRefGoogle Scholar
  15. Castellanos-Gell J, Robainas-Barcia A, Casane D, Chevalier-Monteagudo P, Pina-Amargós F, García-Machado E (2012) The surgeonfish, Acanthurus bahianus, has crossed the Amazon-Orinoco outflow barrier. Mar Biol 159:1561–1565. doi: 10.1007/s00227-012-1942-5 CrossRefGoogle Scholar
  16. Christie MR, Johnson DW, Stallings CD, Hixon MA (2010) Self-recruitment and sweepstakes reproduction amid extensive gene flow in a coral-reef fish. Mol Ecol 19:1042–1057. doi: 10.1111/j.1365-294X.2010.04524.x CrossRefGoogle Scholar
  17. Claro R (ed) (1994) Ecología de los peces marinos de Cuba. Centro de Investigaciones de Quintana Roo, CIQR, MexicoGoogle Scholar
  18. Claro R, García-Arteaga JP, Bouchon-Navarro Y, Louis M, Bouchon C (1998) Características de la estructura de las comunidades de peces en los arrecifes de Las Antillas Menores y Cuba. Avicennia 8:69–86Google Scholar
  19. Claro R, Reshetnikov YS, Alcolado PM (2001) Physical attributes of coastal Cuba. In: Claro R, Lindeman KC, Parenti LR (eds) Ecology of the marine fishes of Cuba. Smithsonian Institution Press, Washington, pp 1–20Google Scholar
  20. Clements KD, Gray RD, Howard Choat J (2003) Rapid evolutionary divergences in reef fishes of the family Acanthuridae (Perciformes: Teleostei). Mol Phylogenet Evol 26:190–201. doi: 10.1016/S1055-7903(02)00325-1 CrossRefGoogle Scholar
  21. Colin PL, Clavijo IE (1988) Spawning activity of fishes producing pelagic eggs on a shelf edge coral reef, south-western Puerto Rico. Bull Mar Sci 43:249–279Google Scholar
  22. Cowen RK, Castro LR (1994) Relation of coral reef fish larval distributions to island scale circulation around Barbados, West Indies. Bull Mar Sci 54:228–244Google Scholar
  23. Cowen RK, Kamazima MML, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287:857–859. doi: 10.1126/science.287.5454.857 CrossRefGoogle Scholar
  24. Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527CrossRefGoogle Scholar
  25. D’Aloia CC, Bogdanowicz SM, Harrison RG, Buston PM (2014) Seascape continuity plays an important role in determining patterns of spatial genetic structure in a coral reef fish. Mol Ecol 23:2902–2913. doi: 10.1111/mec.12782 CrossRefGoogle Scholar
  26. Damerau M, Matschiner M, Salzburger W, Hanel R (2014) Population divergences despite long pelagic larval stages: lessons from crocodile icefishes (Channichthyidae). Mol Ecol 23:284–299. doi: 10.1111/mec.12612 CrossRefGoogle Scholar
  27. DeWoody JA, Avise JC (2000) Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J Fish Biol 56:461–473. doi: 10.1006/jfbi.1999.1210 CrossRefGoogle Scholar
  28. Diaz-Ferguson E, Haney R, Wares J, Silliman B (2010) Population genetics of a trochid gastropod broadens picture of Caribbean Sea connectivity. PLoS ONE 5:e12675. doi: 10.1371/journal.pone.0012675 CrossRefGoogle Scholar
  29. DiBattista JD, Rocha LA, Craig MT, Feldheim KA, Bowen BW (2012) Phylogeography of two closely related indo-pacific butterflyfishes reveals divergent evolutionary histories and discordant results from mtDNA and microsatellites. J Hered 103:1–13. doi: 10.1093/jhered/ess056 CrossRefGoogle Scholar
  30. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Gen Resour 4:359–361. doi: 10.1007/s12686-011-9548-7 CrossRefGoogle Scholar
  31. Eble JA, Toonen RJ, Bowen BW (2009) Endemism and dispersal: comparative phylogeography of three surgeonfishes across the Hawaiian Archipelago. Mar Biol 156:689–698. doi: 10.1007/s00227-008-1119-4 CrossRefGoogle Scholar
  32. Eble JA, Rocha LA, Craig MT, Bowen BW (2011) Not all larvae stay close to home: insights into marine population connectivity with a focus on the brown surgeonfish (Acanthurus nigrofuscus). J Mar Biol. doi: 10.1155/2011/518516 Google Scholar
  33. Espinosa G, Díaz R, Matos J, Becquer U, Romo J, Borrell Y (2003) Variación aloenzimática en poblaciones cubanas del camarón blanco Litopenaeus schmitti. Rev Invest Mar 24:11–19Google Scholar
  34. 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. doi: 10.1111/j.1365-294X.2005.02553.x CrossRefGoogle Scholar
  35. 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 10:564–567CrossRefGoogle Scholar
  36. 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
  37. Eytan RI, Hellberg ME (2010) Nuclear and mitochondrial sequence data reveal and conceal different demographic histories and population genetic processes in Caribbean reef fishes. Evolution 64:3380–3397. doi: 10.1111/j.1558-5646.2010.01071.x CrossRefGoogle Scholar
  38. Foster NL et al (2012) Connectivity of Caribbean coral populations: complementary insights from empirical and modelled gene flow. Mol Ecol 21:1143–1157CrossRefGoogle Scholar
  39. Fu YX (1997) Statistical test of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925Google Scholar
  40. Galarza JA, Carreras-Carbonell J, Macpherson E, Pascual M, Roques S, Turner GF, Rico C (2009) The influence of oceanographic fronts and early-life-history traits on connectivity among littoral fish species. Proc Natl Acad Sci USA 106:1473–1478. doi: 10.1073/pnas.0806804106 CrossRefGoogle Scholar
  41. García-Cagides A, Claro R, Koshelev YBV (1994) Reproducción. In: Claro R (ed) Ecología de los peces marinos de Cuba. Centro de Investigaciones de Quintana Roo, CIQR, Mexico, pp 187–209Google Scholar
  42. García-Machado E, Robainas A, Espinosa G, Páez J, Verdecia N, Monnerot M (2001) Allozyme and mitochondrial DNA variation in Cuban populations of the shrimp Farfantepenaeus notialis (Crustacea:Decapoda). Mar Biol 138:701–707CrossRefGoogle Scholar
  43. González-Sansón G, Aguilar C (2003) Variaciones espaciales y temporales en la abundancia de las especies domunantes de peces de arrecife de coral en la costa de Ciudad de La Habana, Cuba. Rev Invest Mar 24:99–110Google Scholar
  44. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html
  45. Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426CrossRefGoogle Scholar
  46. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. doi: 10.1080/10635150390235520 CrossRefGoogle Scholar
  47. Haug GH, Tiedemann R (1998) Effect of the formation of the Isthmus of Panama on Atlantic Ocean thermohaline circulation. Nature 393:673–676CrossRefGoogle Scholar
  48. Hedgecock D (1994) Does variance in reproductive success limit effective population sizes of marine organisms? In: Beaumont AR (ed) Genetic and evolution of aquatic organisms. Chapman & Hall, London, pp 122–134Google Scholar
  49. Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638CrossRefGoogle Scholar
  50. Heller R, Siegismund HR (2009) Relationship between three measures of genetic differentiation GST, DEST and G’ST: how wrong have we been? Mol Ecol 18:2080–2083. doi: 10.1111/j.1365-294X.2009.04185.x CrossRefGoogle Scholar
  51. Hepburn RI, Sale PF, Dixon B, Heath DD (2009) Genetic structure of juvenile cohorts of bicolor damselfish (Stegastes partitus) along the Mesoamerican barrier reef: chaos through time. Coral Reefs 28:277–288. doi: 10.1007/s00338-008-0423-2 CrossRefGoogle Scholar
  52. Hofmann EE, Worley SJ (1986) An investigation of the circulation of the Gulf of Mexico. J Geophys Res 91:14221–14236CrossRefGoogle Scholar
  53. Hogan JD, Thiessen RJ, Heath DD (2010) Variability in connectivity indicated by chaotic genetic patchiness within and among populations of a marine fish. Mar Ecol Prog Ser 417:263–275. doi: 10.3354/meps08793 CrossRefGoogle Scholar
  54. Hogan JD, Thiessen RJ, Sale PF, Heath DD (2012) Local retention, dispersal and fluctuating connectivity among populations of a coral reef fish. Oecologia 168:61–71. doi: 10.1007/s00442-011-2058-1 CrossRefGoogle Scholar
  55. Horne JB, Lv H, Choat JH, Robertson DR (2008) High population connectivity across the Indo-Pacific: congruent lack of phylogeographic structure in three reef fish congeners. Mol Phylogenet Evol 49:629–638. doi: 10.1016/j.ympev.2008.08.023 CrossRefGoogle Scholar
  56. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332. doi: 10.1111/j.1755-0998.2009.02591.x CrossRefGoogle Scholar
  57. Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011–2014Google Scholar
  58. Hudson RR, Boos DD, Kaplan NL (1992) A statistical test for detecting geographic subdivision. Mol Biol Evol 9:138–151Google Scholar
  59. Klanten OS, Choat JH, Lv H (2007) Extreme genetic diversity and temporal rather than spatial partitioning in a widely distributed coral reef fish. Mar Biol 150:659–670. doi: 10.1007/s00227-006-0372-7 CrossRefGoogle Scholar
  60. Kuhner MK (2006) LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768–770CrossRefGoogle Scholar
  61. Lee WJ, Conroy J, Howell WH, Kocher TD (1995) Structure and evolution of teleost mitochondrial control regions. J Mol Evol 41:54–66CrossRefGoogle Scholar
  62. Leis JM (1991) The pelagic stage of reef fishes: the larval biology of coral reef fishes. In: Sale PF (ed) The ecology of fishes on coral reefs. Academic Press Inc., San Diego, p 725Google Scholar
  63. Leis JM, Rennis DS (1983) The larvae of Indo-Pacific coral reef fishes. University of Hawaii Press, HonoluluGoogle Scholar
  64. Lessa EP (1990) Multidimensional analysis of geographic genetic structure. Syst Zool 39:242–252CrossRefGoogle Scholar
  65. Lessios HA, Robertson DR (2006) Crossing the impassable: genetic connections in 20 reef fishes across the eastern Pacific barrier. Proc R Soc B 273:2201–2208. doi: 10.1098/rspb.2006.3543 CrossRefGoogle Scholar
  66. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefGoogle Scholar
  67. Lindeman KC, Lee TN, Wilson WD, Claro R, Ault JS (2001) Transport of larvae originating in Southewest Cuba and the Dry Tortugas: evidence for partial retention in grunts and snappers. Proc Gulf Caribb Fish Inst 52:732–747Google Scholar
  68. Mantel NA (1967) The detection of disease clustering and generalized regression approach. Cancer Res 27:209–218Google Scholar
  69. McCartney MA, Keller G, Lessios HA (2000) Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Mol Ecol 9:1391–1400CrossRefGoogle Scholar
  70. McCusker MR, Bentzen P (2010) Positive relationships between genetic diversity and abundance in fishes. Mol Ecol 19:4852–4862. doi: 10.1111/j.1365-294X.2010.04822.x CrossRefGoogle Scholar
  71. Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402CrossRefGoogle Scholar
  72. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590Google Scholar
  73. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  74. Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:146–158. doi: 10.1890/1051-0761 CrossRefGoogle Scholar
  75. Paris CB, Cowen RK, Claro R, Lindeman KC (2005) Larvae transport pathways from Cuban snapper (Lutjanidae) spawning aggregations based on biophysical modeling. Mar Ecol Prog Ser 296:93–106. doi: 10.3354/meps296093 CrossRefGoogle Scholar
  76. Pianka ER (1978) Evolutionary ecology. Harper and Row, New YorkGoogle Scholar
  77. Pillans B, Chappell J, Naish TR (1998) A review of the Milankovitch climatic beat: template for Plio-Pleistocene sea-level changes and sequence stratigraphy. Sediment Geol 122:5–21Google Scholar
  78. Planes S, Galzin R, Bonhomme F (1996) A genetic metapopulation model for reef fishes in oceanic islands: the case of the surgeonfish, Acanthurus triostegus. J Evol Biol 9:103–117. doi: 10.1046/j.1420-9101.1996.9010103.x CrossRefGoogle Scholar
  79. Polzin T, Daneschmand SV (2003) On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett 31:12–20CrossRefGoogle Scholar
  80. Portnoy DS, Hollenbeck CM, Renshaw MA, Cummings NJ, Gold JR (2013) Does mating behaviour affect connectivity in marine fishes? Comparative population genetics of two protogynous groupers (Family Serranidae). Mol Ecol 22:301–313. doi: 10.1111/mec.12128 CrossRefGoogle Scholar
  81. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefGoogle Scholar
  82. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959Google Scholar
  83. Puebla O, Bermingham E, McMillan WO (2012) On the spatial scale of dispersal in coral reef fishes. Mol Ecol 21:5675–5688. doi: 10.1111/j.1365-294X.2012.05734.x CrossRefGoogle Scholar
  84. 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 273:1483–1490. doi: 10.1098/rspb.2006.3470 CrossRefGoogle Scholar
  85. Purcell JFH, Cowen RK, Hughes CR, Williams DA (2009) Population structure in a common Caribbean coral-reef fish: implications for larval dispersal and early life-history traits. J Fish Biol 74:403–417. doi: 10.1111/j.1095-8649.2008.02078.x CrossRefGoogle Scholar
  86. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100CrossRefGoogle Scholar
  87. Randall JE (1961) A contribution to the biology of the convict surgeonfish of the Hawaii Islands, Acanthurus triostegus sandvicensis. Pac Sci 15:215–272Google Scholar
  88. Raymo ME (1994) The initiation of Northern Hemisphere glaciation. Annu Rev Earth Planet Sci 22:353–383. doi: 10.1146/annurev.ea.22.050194.002033 CrossRefGoogle Scholar
  89. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  90. Riginos C, Nachman MW (2001) Population subdivision in marine environments: the contributions of biogeography, geographical distance and discontinuous habitat to genetic differentiation in a blennioid fish, Axoclinus nigricaudus. Mol Ecol 10:1439–1453. doi: 10.1046/j.1365-294X.2001.01294.x CrossRefGoogle Scholar
  91. Riginos C, Douglas KE, Jin Y, Shanahan DF, Treml EA (2011) Effects of geography and life history traits on genetic differentiation in benthic marine fishes. Ecography 34:566–575CrossRefGoogle Scholar
  92. Riginos C, Buckley YM, Blomberg SP, Treml EA (2014) Dispersal capacity predicts both population genetic structure and species richness in reef fishes. Am Nat 184:52–64. doi: 10.1086/676505 CrossRefGoogle Scholar
  93. Robainas A, Espinosa G, Hernández D, García-Machado E (2005) Temporal variation of the population structure and genetic diversity of Farfantepenaeus notialis assessed by allozyme loci. Mol Ecol 14:2933–2942. doi: 10.1111/j.1365-294X.2005.02613.x CrossRefGoogle Scholar
  94. Robertson DR (1985) Sexual-size dimorphism in surgeon fishes. In: Proceedings of the 5th International Congress on Coral Reefs, vol 5, pp 403–408Google Scholar
  95. Robertson DR (1990) Differences in the seasonalities of spawning and recruitment of some small neotropical reef fishes. J Exp Mar Biol Ecol 144:49–62. doi: 10.1016/0022-0981(90)90019-9 CrossRefGoogle Scholar
  96. Robertson DR, Green DG, Victor BC (1988) Temporal coupling of production and recruitment of larvae of a caribbean reef fish. Ecology 69:370–381. doi: 10.2307/1940435 CrossRefGoogle Scholar
  97. Robertson DR, Ackerman JL, Choat JH, Posada JM, Pitt J (2005) Ocean surgeonfish Acanthurus bahianus. I. The geography of demography. Mar Ecol Prog Ser 295:229–244. doi: 10.3354/meps295229 CrossRefGoogle Scholar
  98. 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. doi: 10.1046/j.0962-1083.2001.01431.x CrossRefGoogle Scholar
  99. Rocha LA, Robertson DR, Roman J, Bowen BW (2005) Ecological speciation in tropical reef fishes. Proc R Soc B 272:573–579. doi: 10.1098/2004.3005 CrossRefGoogle Scholar
  100. Rocha LA, Rocha CR, Robertson DR, Bowen BW (2008) Comparative phylogeography of Atlantic reef fishes indicates both origin and accumulation of diversity in the Caribbean. BMC Evol Biol 8:157. doi: 10.1186/1471-2148-8-157 CrossRefGoogle Scholar
  101. Roff DA, Bentzen P (1989) The statistical analysis of mitochondrial DNA polymorphisms: X 2 and the problem of small samples. Mol Biol Evol 6:539–545Google Scholar
  102. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569Google Scholar
  103. Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106. doi: 10.1111/j.1471-8286.2007.01931.x CrossRefGoogle Scholar
  104. Salas E, Molina-Ureña H, Walter RP, Heath DD (2010) Local and regional genetic connectivity in a Caribbean coral reef fish. Mar Biol 157:437–445. doi: 10.1007/s00227-009-1330-y CrossRefGoogle Scholar
  105. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning—a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  106. Schlueter MA (1998) Population genetic structure and gene flow within three coral reef fish species in the Florida Keys. Dissertation, Miami UniversityGoogle Scholar
  107. Schmidt D, Pool J (2002) The effect of population history on the distribution of the Tajima’s D statistic. Cornell University Press, Ithaca, p 8Google Scholar
  108. Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rate vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089Google Scholar
  109. Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464CrossRefGoogle Scholar
  110. Selkoe KA, Toonen RJ (2011) Marine connectivity: a new look at pelagic larval duration and genetic metrics of dispersal. Mar Ecol Prog Ser 436:291–305. doi: 10.3354/meps09238 CrossRefGoogle Scholar
  111. Severance EG, Karl SA (2006) Contrasting population genetic structures of sympatric, mass-spawning Caribbean corals. Mar Biol. doi: 10.1007/s00227-006-0332-2 Google Scholar
  112. Shulman MJ, Bermingham E (1995) Early life histories, ocean currents, and the population genetics of Caribbean reef fishes. Evolution 49:897–910CrossRefGoogle Scholar
  113. Sponaugle S, Cowen RK (1996) Larval supply and patterns of recruitment for two caribbean reef fishes, Stegastes partitus and Acanthurus bahianus. Mar Freshw Res 47:433–447CrossRefGoogle Scholar
  114. Sponaugle S, Fortuna J, Grorud K, Lee T (2003) Dynamics of larval fish assemblages over a shallow coral reef in the Florida Keys. Mar Biol 143:175–189CrossRefGoogle Scholar
  115. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595Google Scholar
  116. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526Google Scholar
  117. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  118. Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109CrossRefGoogle Scholar
  119. Taylor MS, Hellberg ME (2006) Comparative phylogeography in a genus of coral reef fishes: biogeographic and genetic concordance in the Caribbean. Mol Ecol 15:695–707. doi: 10.1111/j.1365-294X.2006.02820.x CrossRefGoogle Scholar
  120. Valdés-Muñoz E, Mochek AD (1994) Estructura etológica de las comunidades de peces. In: Claro R (ed) Ecología de los peces marinos de Cuba. Centro de Investigaciones de Quintana Roo, CIQR, Mexico, pp 143–162Google Scholar
  121. Valdés-Muñoz E, Mochek AD (2001) Behavior of the marine fishes of the Cuban shelf. In: Claro R, Lindeman KC, Parenti LR (eds) Ecology of the marine fishes of Cuba. Smithsonian Institution Press, Washington, pp 58–71Google Scholar
  122. 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 4:535–538CrossRefGoogle Scholar
  123. Victoria del Río I, Penié I (1998) Hidrología. In: Vales M, Alvarez A, Montes L, Avila A (eds) Estudio nacional sobre la diversidad biológica en la República de Cuba. PNUMA/CENBIO/IES/AMA/CITMA, La Habana, pp 117–125Google Scholar
  124. Villegas-Hernández H, González-Salas C, Aguilar-Perera A, López-Gómez MJ (2008) Settlement dynamics of the coral reef fish Stegastes partitus, inferred from otolith shape and microstructure analysis. Aquat Biol 1:249–258. doi: 10.3354/ab00026 CrossRefGoogle Scholar
  125. Villegas-Sánchez CA, Rivera-Madrid R, Arias-González JE (2010) Small-scale genetic connectivity of bicolor damselfish (Stegastes partitus) recruits in Mexican Caribbean reefs. Coral Reefs 29:1023–1033. doi: 10.1007/s00338-010-0643-0 CrossRefGoogle Scholar
  126. Vollmer SV, Palumbi SR (2007) Restricted gene flow in the caribbean staghorn coral Acropora cervicornis: implications for the recovery of endangered reefs. J Hered 98:40–50CrossRefGoogle Scholar
  127. Wang IJ (2010) Recognizing the temporal distinctions between landscape genetics and phylogeography. Mol Ecol 19:2605–2608. doi: 10.1111/j.1365-294X.2010.04715.x CrossRefGoogle Scholar
  128. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  129. Wellington GM, Victor BC (1989) Planktonic larval duration of one hundred species of Pacific and Atlantic damselfishes (Pomacentridae). Mar Biol 101:557–567CrossRefGoogle Scholar
  130. White C, Selkoe KA, Watson J, Siegel DA, Zacherl DC, Toonen RJ (2010) Ocean currents help explain population genetic structure. Proc R Soc B 277:1685–1694. doi: 10.1098/rspb.2009.2214 CrossRefGoogle Scholar
  131. Williams DA, Purcell J, Hughes CR, Cowen RK (2003) Polymorphic microsatellite loci for population studies of the bicolor damselfish, Stegastes partitus (Pomacentridae). Mol Ecol Notes 3:547–549CrossRefGoogle Scholar
  132. Williams DA, Purcell J, Cowen RK, Hughes CR (2004) Microsatellite multiplexes for high-throughput genotyping of French grunts (Haemulon flavolineatum, Pisces: Haemulidae) and their utility in other grunt species. Mol Ecol Notes 4:46–48CrossRefGoogle Scholar
  133. Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395–420CrossRefGoogle Scholar
  134. Zaykin DV, Pudovkin AI (1993) Two programs to estimate significance of X 2 values using pseudo-probability test. J Hered 84:152Google Scholar
  135. Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121. doi: 10.1111/j.1365-294X.2008.03737.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Jessy Castellanos-Gell
    • 1
    Email author
  • Aymée Robainas-Barcia
    • 2
  • Fabián Pina-Amargós
    • 3
  • Pedro Chevalier-Monteagudo
    • 4
  • Cushla Metcalfe
    • 5
  • Wagner Franco Molina
    • 6
  • Didier Casane
    • 7
    • 8
  • Erik García-Machado
    • 1
    Email author
  1. 1.Centro de Investigaciones MarinasUniversidad de La HabanaPlayaCuba
  2. 2.Pierre Fabre IbericaBarcelonaSpain
  3. 3.Centro de Investigaciones de Ecosistemas CosterosCayo Coco, MorónCuba
  4. 4.Acuario Nacional de CubaPlayaCuba
  5. 5.CSIROSt LuciaAustralia
  6. 6.Departamento de Biologia Celular e Genética, Centro de BiociênciasUniversidade Federal do Rio Grande do NorteNatalBrazil
  7. 7.Evolution, Génomes, Comportement and Ecologie, CNRS, IRDUniv. Paris-Sud, Université Paris-SaclayGif-sur-YvetteFrance
  8. 8.Université Paris DiderotParisFrance

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