Marine Biology

, Volume 150, Issue 6, pp 1321–1332 | Cite as

Population structure of red porgy, Pagrus pagrus, in the Atlantic Ocean

  • A. O. Ball
  • M. G. Beal
  • R. W. ChapmanEmail author
  • G. R. Sedberry
Research Article


The red porgy, Pagrus pagrus (L.), is a protogynous sparid associated with reefs and hard bottom habitat throughout the warm-temperate Atlantic Ocean. In this study, the degree of geographic population differentiation in Atlantic populations was examined with microsatellite and mitochondrial DNA markers (mtDNA). Six microsatellite loci were amplified and scored in 690 individuals from the eastern North Atlantic (Crete, Madeira, and Azores), western North Atlantic (North Carolina to Florida, and the eastern Gulf of Mexico), and Brazil. At two loci, fixed allelic differences were found among the three major geographic areas, while frequency differences were observed at three other loci. The DNA of 371 individuals was amplified at the mtDNA control region, and 526 bp were sequenced. Tamura–Nei’s D was used as a measure of nucleotide diversity and divergence: diversity averaged 0.011 within samples, while the corrected divergence averaged 0 between samples within the same area and 0.061 between samples from different areas. Transversion haplotype minimum spanning networks, nucleotide divergence, and FST values all show that the western Atlantic samples were more closely related to each other than any was to samples from the eastern North Atlantic. Within the western North Atlantic, no significant population differentiation was observed, and within the eastern North Atlantic, only the Azores sample showed detectable differences from Crete and Madeira. These data indicate general homogeneity within large areas, and deep divisions between these areas.


Control Region Reef Fish Mismatch Distribution Control Region Sequence Atlantic 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.



The authors thank Jorge Kotas, Centro de Pesquisa e Extensão Pesqueira das Regiões Sudeste e Sul, Instituto do Meio Ambiente e dos Recursos Naturais Renováveis for Brazilian samples; Carlos Andrade, Direcção Regional das Pescas, Madeira and Gui Menezes, Departamento de Oceanografia e Pescas, Azores, for eastern Atlantic samples; and Antonios Magoulas, Hellenic Centre for Marine Research, Crete, for Crete samples. Patrick Harris made significant contributions to discussions of life history and fisheries, and two anonymous reviewers provided useful comments. This is Contribution no. 587 of the South Carolina Marine Resources Center. The experimental procedures complied with current national laws.

Supplementary material

227_2006_425_MOESM1_ESM.doc (42 kb)
Supplementary material


  1. Aboim MA, Menezes GM, Schlitt T, Rogers AD (2005) Genetic structure and history of populations of the deep-sea fish Helicolenus dactylopterus (Delaroche, 1809) inferred from mtDNA sequence analysis. Mol Ecol 14:1343–1354PubMedGoogle Scholar
  2. Adcock GJ, Bernal Ramírez JH, Hauser L, Smith P, Carvalho GR (2000) Screening of DNA polymorphisms in samples of archived scales from New Zealand snapper. J Fish Biol 56:1283–1287Google Scholar
  3. Allendorf FW, Phelps SR (1981) Use of allelic frequencies to describe population structure. Can J Fish Aquat Sci 38:1507–1514Google Scholar
  4. Allmon WD (2001) Nutrients, temperature, disturbance, and evolution: a model for the late Cenozoic marine record of the western Atlantic. Palaeogeogr Palaeoclimatol Palaeoecol 166:9–26Google Scholar
  5. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  6. Bagley MJ, Lindquist DG, Geller JB (1999) Microsatellite variation, effective population size, and population genetic structure of vermilion snapper, Rhomboplites aurorubens, off the southeastern USA. Mar Biol 134:609–620Google Scholar
  7. Ball AO, Chapman RW (2003) Population genetic analysis of white shrimp, Litopenaeus setiferus, using microsatellite genetic markers. Mol Ecol 12:2319–2330PubMedGoogle Scholar
  8. Ball AO, Sedberry GR, Wessel JH, III, Chapman RW (2003) Large-scale genetic differentiation of Pagrus pagrus in the Atlantic. J Fish Biol 62:1232–1237Google Scholar
  9. Ball AO, Sedberry GR, Zatcoff MS, Chapman RW, Carlin JL (2000) Population structure of the wreckfish Polyprion americanus determined with microsatellite genetic markers. Mar Biol 137:1077–1090Google Scholar
  10. Barans CA, Henry VJ Jr (1984) A description of the shelf edge groundfish habitat along the southeastern United States. NE Gulf Sci 7:77–96Google Scholar
  11. Bargelloni L, Alarcon JA, Alvarez MC, Penzo E, Magoulas A, Reis C, Patarnello T (2003) Discord in the family Sparidae (Teleostei): divergent phylogeographical patterns across the Atlantic–Mediterranean divide. J Evol Biol 16:1149–1158PubMedGoogle Scholar
  12. Batargias C, Dermitzakis E, Magoulas A, Zouros E (1999) Characterization of six polymorphic microsatellite markers in gilthead seabream, Sparus aurata (Linnaeus 1758). Mol Ecol 8:897–898PubMedGoogle Scholar
  13. Bauchot M-L, Hureau JC (1990) Sparidae. In: Quero JC, Hureau JC, Karrer C, Post A, Saldanha L (eds) Check-list of the fishes of the eastern tropical Atlantic (CLOFETA). JNICT, Lisbon, SEI, Paris, UNESCO, Paris, pp 808–809Google Scholar
  14. Beaumariage DS (1969) Returns from the 1965 Schlitz tagging program, including a cumulative analysis of previous results. Marine Research Laboratory, Florida Department of Natural Resources, Division of Marine Resources, St. PetersburgGoogle Scholar
  15. Berggren WA, Hollister CD (1974) Paleogeography, paleobiogeography, and the history of circulation in the Atlantic Ocean. In: Hay WW (ed) Studies in paleo-oceanography. Soc. Economic Paleontology Mineralogy, Special Publication, no. 20, pp 126–186Google Scholar
  16. Bernal-Ramírez JH, Adcock GJ, Hauser L, Carvalho GR, Smith PJ (2003) Temporal stability of genetic population structure in the New Zealand snapper, Pagrus auratus, and relationship to coastal currents. Mar Biol 142:567–574Google Scholar
  17. Bernardi G, Holbrook SJ, Schmitt RJ (2001) Gene flow at three spatial scales in a coral reef fish, the three-spot dascyllus, Dascyllus trimaculatus. Mar Biol 138:457–465Google Scholar
  18. Bowen BW, Bass AL, Rocha LA, Grant WS, Robertson DR (2001) Phylogeography of the trumpetfishes (Aulostomus): ring species complex on a global scale. Evolution 55:1029–1039PubMedGoogle Scholar
  19. Briggs JC (1974) Marine zoogeography. McGraw-Hill, New YorkGoogle Scholar
  20. Brown JR, Beckenbach AT, Smith MJ (1993) Intraspecific DNA sequence variation of the mitochondrial control region of white sturgeon (Acipenser transmontanus). Mol Biol Evol 10:326–341PubMedGoogle Scholar
  21. Brown WM, George M Jr, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76:1967–1971PubMedGoogle Scholar
  22. Carlin JL, Robertson DR, Bowen BW (2003) Ancient divergences and recent connections in two tropical Atlantic reef fishes Epinephelus adscensionis and Rypticus saponaceous (Percoidei: Serranidae). Mar Biol 143:1057–1069Google Scholar
  23. Castro BM, Miranda LB (1998) Physical oceanography of the Wesern Atlantic continental shelf located between 4°N and 24°S. In: Robinson AR, Brink KH (eds) The sea. Wiley, New York, pp 209–251Google Scholar
  24. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolution 21:550–570PubMedGoogle Scholar
  25. Cronin TM, Dowsett HJ (1996) Biotic and oceanographic response to the Pliocene closing of the Central American isthmus. In: Jackson JBC, Budd AF, Coates AG (eds) Evolution and environment in tropical America. University of Chicago Press, Chicago, pp 76–104Google Scholar
  26. Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864PubMedGoogle Scholar
  27. Excoffier L, Laval G, Schneider S (2005) Arlequin (ver. 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  28. Fauvelot C, Planes S (2002) Understanding origins of present-day genetic structure in marine fish: biologically or historically driven patterns? Mar Biol 141:773–788Google Scholar
  29. Felsenstein J (1993) PHYLIP (Phylogeny Inference Package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington, SeattleGoogle Scholar
  30. Fisher RA (1970) Statistical methods for research workers. Oliver and Boyd, EdinburghGoogle Scholar
  31. Ginsburg I (1952) Eight new fishes from the Gulf coast of the United States, with two new genera and notes on geographic distribution. J Wash Acad Sci 42:84–101Google Scholar
  32. Gonzalez-Silvera A, Santamaria-del-Angel E, Garcia VMT, Carlos CAE, Garcia AE, Millán-Nuñez R, Muller-Karger F (2004) Biogeographical regions of the tropical and subtropical Atlantic Ocean off South America: classification based on pigment (CZCS) and chlorophyll-a (SeaWiFS) variability. Cont Shelf Res 24:983–1000Google Scholar
  33. Guarniero I, Franzellitti S, Ungaro N, Tommasini S, Piccinetti C, Tinti F (2002) Control region haplotype variation in the central Mediterranean common sole indicates geographical isolation and population structuring in Italian stocks. J Fish Biol 60:1459–1474Google Scholar
  34. Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372PubMedGoogle Scholar
  35. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  36. Hanel R, Sturmbauer C (2000) Multiple recurrent evolution of trophic types in northeastern Atlantic and Mediterranean seabreams (Sparidae, Percoidei). J Mol Evol 50:276–283PubMedGoogle Scholar
  37. Harris PJ, McGovern JC (1997) Changes in the life history of red porgy, Pagrus pagrus, from the southeastern United States, 1972–1994. Fish Bull 95:732–747Google Scholar
  38. Haug GH, Tiedemann R (1998) Effect of the formation of the Isthmus of Panama on Atlantic Ocean thermohaline circulation. Nature 393:673–676Google Scholar
  39. Hauser L, Ward RD (1998) Population identification in pelagic fish: the limits of molecular markers. In: Carvalho GR (ed) Advances in Molecular Ecology. NATO Advanced Science Institutes Series, series A, life sciences. IOS Press, Amsterdam, pp 191–224Google Scholar
  40. Hoffman EA, Kolm N, Berglund A, Arguello JR, Jones AG (2005) Genetic structure in the coral-reef-associated Banggai cardinalfish, Pterapogon kauderni. Mol Ecol 14:1367–1375PubMedGoogle Scholar
  41. Holmquist R (1983) Transitions and transversions in evolutionary descent: an approach to understanding. J Mol Evol 19:134–144PubMedGoogle Scholar
  42. Hood PB, Johnson AK (2000) Age, growth, mortality, and reproduction of red porgy, Pagrus pagrus, from the eastern Gulf of Mexico. Fish Bull 98:723–735Google Scholar
  43. Hudson RR (1990) Gene genealogies and the coalescent process. In: Futuyama D, Antonovics JD (eds) Oxford surveys in evolutionary biology. Oxford University Press, New York, pp 1–44Google Scholar
  44. Jansen JHF, Kuijpers A, Troelstra SR (1986) A mid-Brunhes climatic event: long-term changes in global atmosphere and ccean circulation. Science 232:619–622PubMedGoogle Scholar
  45. Jones GP, Millicich MJ, Emslie MJ, Lunow C (1999) Self-recruitment in a coral reef fish population. Nature 402:802–804Google Scholar
  46. Joyeux J-C, Floeter SR, Ferreira CEL, Gasparini JL (2001) Biogeography of tropical reef fishes: the South Atlantic puzzle. J Biogeogr 28:831–841Google Scholar
  47. Kaneps AG (1979) Gulf Stream: velocity fluctuations during the late Cenozoic. Science 204:297–301PubMedGoogle Scholar
  48. Keigwin L (1982) Isotopic paleoceanography of the Caribbean and East Pacific: role of Panama uplift in late Neogene time. Science 217:350–353PubMedGoogle Scholar
  49. Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738PubMedPubMedCentralGoogle Scholar
  50. Kruskal JB (1956) On the shortest spanning subtree of a graph and the traveling salesman problem. Proc Am Math Soc 7:48–50Google Scholar
  51. Kumar S, Gadagkar SR (2000) Efficiency of the neighbor-joining method in reconstructing deep and shallow evolutionary relationships in large phylogenies. J Mol Evol 51:544–553PubMedGoogle Scholar
  52. Labropoulou M, Machias A, Tsimenides N (1999) Habitat selection and diet of juvenile red porgy, Pagrus pagrus (Linnaeus, 1758). Fish Bull 97:495–507Google Scholar
  53. Lee W-J, Conroy J, Howell WH, Kocher TD (1995) Structure and evolution of teleost mitochondrial control regions. J Mol Evol 41:54–66PubMedGoogle Scholar
  54. Levene H (1949) On a matching problem arising in genetics. Ann Math Stat 20:91–94Google Scholar
  55. Lloris D, Rucabado J, Figueroa H (1991) Biogeography of the Macaronesian ichthyofauna (the Azores, Madeira, the Canary Islands, Cape Verde and the African enclave). Bol Mus Mun Funchal 43:191–241Google Scholar
  56. Maier-Reimer E, Mikolajewicz U, Crowley T (1990) Ocean general circulation model sensitivity experiment with an open Central American isthmus. Paleoceanography 5:349–366Google Scholar
  57. Manooch CS, III, Hassler WW (1978) Synopsis of biological data on the red porgy, Pagrus pagrus (Linnaeus). NOAA technical report NMFS circular 412, US Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries ServiceGoogle Scholar
  58. Manooch CS, III, Huntsman GR, Sullivan B, Elliott J (1976) Conspecific status of the sparid fishes Pagrus sedecim Ginsburg and Pagrus pagrus Linnaeus. Copeia 1976:678–684Google Scholar
  59. Martin AP, Palumbi SR (1993) Body size, metabolic rate, generation time, and the molecular clock. Proc Natl Acad Sci USA 90:4087–4091Google Scholar
  60. Martin AP, Humphreys R, Palumbi SR (1992) Population genetic structure of the armorhead, Pseudopentaceros wheeleri, in the North Pacific Ocean: application of the polymerase chain reaction to fisheries problems. Can J Fish Aquat Sci 49:2386–2391Google Scholar
  61. Mills LS, Allendorf FW (1996) The one-migrant-per-generation rule in conservation and management. Conserv Biol 10:1509–1518Google Scholar
  62. Mudelsee M, Schulz M (1997) The Mid-Pleistocene climate transition: onset of 100 ka cycle lags ice volume build-up by 280 ka. Earth Planet Sci Lett 151:117–123Google Scholar
  63. Muss A, Robertson DR, Stepien CA, Wirtz P, Bowen BW (2001) Phylogeography of Ophioblennius: the role of ocean currents and geography in reef fish evolution. Evolution 55:561–572PubMedGoogle Scholar
  64. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedPubMedCentralGoogle Scholar
  65. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  66. Orrell TM, Carpenter KE, Musick JA, Graves JE (2002) Phylogenetic and biogeographic analysis of the Sparidae (Perciformes: Percoidei) from cytochrome b sequences. Copeia 2002:618–631Google Scholar
  67. Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  68. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572Google Scholar
  69. Parker ROJ (1990) Tagging studies and diver observations of fish populations on live-bottom reefs of the U.S. southeastern coast. Bull Mar Sci 46:749–760Google Scholar
  70. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818Google Scholar
  71. Ranzi S (1969) Sparidae. In: Lo Bianco S (ed) Eggs, larvae and juvenile stages of Teleostei (Uova, larve e stadî giovanili di Teleostei). Fauna and flora of the Bay of Naples. Monograph, no. 38. Translated from Italian by L. Franchetti (translation edited by H. Mills). Jerusalem, IsraelGoogle Scholar
  72. Raymond M, Rousset F (1995a) An exact test for population differentiation. Evolution 49:1280–1283PubMedPubMedCentralGoogle Scholar
  73. Raymond M, Rousset F (1995b) GENEPOP (ver. 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  74. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225PubMedPubMedCentralGoogle Scholar
  75. 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 11:243–251PubMedGoogle Scholar
  76. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569Google Scholar
  77. Rousset F, Raymond M (1995) Testing heterozygote excess and deficiency. Genetics 140:1413–1419PubMedPubMedCentralGoogle Scholar
  78. SAFMC (2003) Report of red porgy stock assessment workshop. South Atlantic Fishery Management Council, CharlestonGoogle Scholar
  79. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  80. Schefuss E, Damsté JSS, Jansen JHF (2004) Forcing of tropical Atlantic sea surface temperatures during the mid-Pleistocene transition. Paleoceanography 19:PA4029Google Scholar
  81. Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089PubMedPubMedCentralGoogle Scholar
  82. Sedberry GR, Carlin JL, Chapman RW, Eleby B (1996) Population structure in the pan-oceanic wreckfish, Polyprion americanus (Teleostei: Polyprionidae), as indicated by mtDNA variation. J.Fish Biol 49(Suppl. A):318–329Google Scholar
  83. Shulman MJ, Bermingham E (1995) Early life histories, ocean currents, and the population genetics of Caribbean reef fishes. Evolution 49:897–910PubMedGoogle Scholar
  84. Stephanou D, Georgiou G, Shoukri E (1995) Reproduction and larval rearing of the common sea bream (Pagrus pagrus), an experimental culture. Marine aquaculture finfish species diversification. Seminar of the CIHEAM network on technology of aquaculture in the Mediterranean. Nicosia (Cyprus)Google Scholar
  85. Summerer M, Hanel R, Sturmbauer C (2001) Mitochondrial phylogeny and biogeographic affinities of sea breams of the genus Diplodus (Sparidae). J Fish Biol 59:1638–1652Google Scholar
  86. Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799–802Google Scholar
  87. Tabata K, Taniguchi N (2000) Differences between Pagrus major and Pagrus auratus through mainly mtDNA control region analysis. Fish Sci 66:9–18Google Scholar
  88. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  89. Takagi M, Taniguichi N, Cook D, Doyle RW (1997) Isolation and characterization of microsatellite loci from red sea bream Pagrus major and detection in closely related species. Fish Sci 63:199–204Google Scholar
  90. 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 10:512–526PubMedPubMedCentralGoogle Scholar
  91. Webb T, III, Bartlein PJ (1992) Global changes during the last 3 million years: climatic controls and biotic responses. Annu Rev Ecol Syst 23:141–173Google Scholar
  92. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370Google Scholar
  93. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159PubMedPubMedCentralGoogle Scholar
  94. Zatcoff MS, Ball AO, Sedberry GR (2004) Population genetic analysis of red grouper, Epinephelus morio, and scamp, Mycteroperca phenax, from the southeastern U.S. Atlantic and Gulf of Mexico. Mar Biol 144:769–777Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • A. O. Ball
    • 1
  • M. G. Beal
    • 1
  • R. W. Chapman
    • 1
    Email author
  • G. R. Sedberry
    • 1
  1. 1.South Carolina Department of Natural ResourcesCharlestonUSA

Personalised recommendations