Marine Biology

, Volume 146, Issue 4, pp 793–804

Genetic population structure in the black-spot sea bream (Pagellus bogaraveo Brünnich, 1768) from the NE Atlantic

  • B. Stockley
  • G. Menezes
  • M. R. Pinho
  • A. D. Rogers
Research Article


The depletion of shallow-water fish stocks through overexploitation has led to increasing fishing pressure on deep-sea species. Poor knowledge of the biology of commercially valuable deep-water fish has led to the serial depletion of stocks of several species across the world. Data regarding the genetic structure of deep-sea fish populations is important in determining the impact of overfishing on the overall genetic variability of species and can be used to estimate the likelihood of recolonisation of damaged populations through immigration of individuals from distant localities. Here the genetic structure of the commercially fished deep-water species the blackspot sea bream, Pagellus bogaraveo is investigated in the northeastern Atlantic using partial DNA sequencing of mitochondrial cytochrome b (cyt-b) and D-loop regions and genotyping of microsatellite loci. An absence of variation in cyt-b and low genetic variation in D-loop sequences potentially indicate that P. bogaraveo may have undergone a severe bottleneck in the past. Similar bottlenecks have been detected in other Atlantic species of fish and have possibly originated from the last glaciation. P. bogaraveo may have been particularly vulnerable to the effects of low temperature and a fall in sea level because stages of its life history occur in shallow water and coastal sites. However, there are other explanations of low genetic variability in populations of P. bogaraveo, such as a low population size and the impacts of fishing on population structure. Analysis of population structure using both D-loop and microsatellite analysis indicates low to moderate, but significant, genetic differentiation between populations at a regional level. This study supports studies on other deep-sea fish species that indicate that hydrographic or topographic barriers prevent dispersal of adults and/or larvae between populations at regional and oceanographic scales. The implications for the management and conservation of deep-sea fish populations are discussed.


  1. Adams J, Maslin M, Thomas E (1999) Sudden climate transitions during the Quaternary. Prog Phys Geogr 23:1–36Google Scholar
  2. Bailey KM, Stabeno PJ, Powers DA (1997) The role of larval retention and transport features in the mortality and potential gene flow of the walleye pollack. J Fish Biol 51 (Suppl A):135–154CrossRefPubMedGoogle Scholar
  3. Baker CS, Perry A, Chambers GK, Smith PJ (1995) Population variation in the mitochondrial cytochrome b gene of the orange roughy Hoplostethus atlanticus and the hoki Macruronus novaezelandiae. Mar Biol 122:503–509CrossRefGoogle Scholar
  4. Bargelloni L, Alarcon JA, Alvarez MC, Penzo E, Margoulas A, Reis C, Patarnello T (2003) Discord in the family Sparidae (Teleostei): divergent phylogeographical patterns across the Atlantic–Mediterranean divide. J Evol Biol 16:1149–1158CrossRefPubMedGoogle Scholar
  5. Barton NH (2000) Genetic hitchhiking. Philos Trans R Soc Lond B Biol Sci 355:1553–1562CrossRefPubMedGoogle Scholar
  6. Bernatchez L, Dodson JJ, Bolvin S (1989) Population bottlenecks—influence on mitochondrial-DNA diversity and its effect on coregonine stock discrimination. J Fish Biol 35 (Suppl A):233–244Google Scholar
  7. Bossart JL, Prowell DP (1998) Genetic estimates of population structure and gene flow: limitations, lessons and new directions. Trends Ecol Evol 13:202–206CrossRefGoogle Scholar
  8. Carr SM, Snellen AJ, Howse KA, Wroblewski JS (1995) Mitochondrial DNA sequence variation and genetic stock structure of Atlantic cod (Gadus morhua) from bay and offshore locations on the Newfoundland continental shelf. Mol Ecol 4:79–88PubMedGoogle Scholar
  9. Carvalho GR, Hauser L (1995) Molecular genetics and the stock concept in fisheries. In: Carvalho GR, Pitcher TJ (eds) Molecular genetics in fisheries. Chapman & Hall, London, pp 55–79Google Scholar
  10. Clark MR (1995) Experience with the management of orange roughy (Hoplostethus atlanticus) in New Zealand and the effects of commercial fishing on stocks over the period 1980–1993. In: Hopper AG (ed) Deep-water fisheries of the North Atlantic oceanic slope. Kluwer, Dordrecht, pp 251–266Google Scholar
  11. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefPubMedGoogle Scholar
  12. Creasey S, Rogers AD (1999) Population genetics of bathyal and abyssal organisms. Adv Mar Biol 35:1–151Google Scholar
  13. Desdevises Y, Jovelin R, Jousson O, Morand S (2000) Comparison of ribosomal DNA sequences of Lamellodiscus spp. (Monogenea, Diplectanidae) parasitising Pagellus (Sparidae, Teleostei) in the north Mediterranean Sea: species divergence and coevolutionary interactions. Int J Parasitol 30:741–746CrossRefPubMedGoogle Scholar
  14. Donaldson KA, Wilson RR (1999) Amphi-panamic geminates of snook (Percoidei: Centropomidae) provide a calibration of the divergence rate in the mitochondrial DNA control region of fishes. Mol Phylogen Evol 13:208–213CrossRefGoogle Scholar
  15. Duschenko VV (1988) The formation of the commercial stock of the north Atlantic grenadier. Can Transl Fish Aquat Sci 5340:1–21Google Scholar
  16. D’yakov YP (1991) Population structure of Pacific black halibut, Reinhardtius hippoglossoides. J Icthyol 31:16–28Google Scholar
  17. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplogroups: applications to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  18. Fauvelot C, Bernardi G, Planes S (2003) Reductions in the mitochondrial DNA diversity of coral reef fish provide evidence of population bottlenecks resulting from Holocene sea-level change. Evolution 57:1571–1583PubMedGoogle Scholar
  19. Fenton GE, Short SA, Ritz DA (1991) Age determination of orange roughy, Hoplostethus atlanticus (Pisces: Trachichthyidae) using 210Pb:226Ra disequilibria. Mar Biol 109:197–202Google Scholar
  20. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeGoogle Scholar
  21. Garcia de Leon F, Chikhi JL, Bonhomme F (1997) Microsatellite polymorphism and population subdivision in natural populations of European sea bass Dicentrachus labrax (Linnaeus, 1758) Mol Ecol 6:51–62Google Scholar
  22. Gianni M (2004) High seas bottom fisheries and their impact on the biodiversity of vulnerable deep-sea ecosystems: summary findings. Report to the World Conservation Union, World Wildlife Fund and Natural Resources Defence Council. IUCN, Gland, Switzerland, pp 1–83Google Scholar
  23. Glenn TC, Stephan W, Braun MJ (1999) Effects of a population bottleneck on whooping crane mitochondrial DNA variation. Conserv Biol 13:1097–1107CrossRefGoogle Scholar
  24. 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 89:415–428CrossRefGoogle Scholar
  25. Guo S, Thompson E (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372PubMedGoogle Scholar
  26. Haedrich RL (1995) Structure over time of an exploited deepwater fish assemblage. In: Hopper AG (ed) Deep-water fisheries of the North Atlantic oceanic slope. Kluwer, Dordrecht, pp 70–96Google Scholar
  27. Hoarau G, Borsa P (2000) Extensive gene flow within sibling species in the deep-sea fish Beryx splendens. C R Acad Sci Sci Vie 323:315–325Google Scholar
  28. Jean C, Hui C, Lee S, Chen C (1995) Variation in the mitochondrial DNA and phylogenetic relationships of fish of the subfamily Sparinae (Perciformes: Sparidae) in the coastal waters of Taiwan. Zool Stud 34:270–280Google Scholar
  29. Karrer C (1984) Beschreibung von Jungenstadien dreier Spariden-Arten aus dem nordwest-afrikanischen Auftriebsgebeit (Teleostei, Perciformes). Arch Fisch Wissenschaft 35:53–90Google Scholar
  30. Kocher TD, Thomas WK, Meyer A, Edwards SV, Paabo S, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci U S A 86:6169–6200Google Scholar
  31. Koslow JA, Boehlert GW, Gordon JDM, Haedrich RL, Lorance P, Parin N (2000) Continental slope and deep-sea fisheries: implications for a fragile ecosystem. ICES J Mar Sci 57:548–557CrossRefGoogle Scholar
  32. Krug H (1998) Variation in the reproductive cycle of the black spot seabream, Pagellus bogaraveo (Brünnich, 1768) in the Azores. Arquipelago Bull Univ Azores Life Mar Sci 16A:37–47Google Scholar
  33. Mace PM, Fenaughty JM, Coburn RP, Doonan IJ (1990) Growth and productivity of orange roughy (Hoplostethus atlanticus) on the north Chatham Rise. N Z J Mar Freshw Res 24:105–119Google Scholar
  34. Martin AP, Humphreys R, Palumbi SR (1992) Population genetic structure of the armourhead, Pseudopentaceros wheeleri, in the North Pacific Ocean: application of the polymerase chain reaction to fisheries populations. Can J Fish Aquat Sci 49:2368–2391Google Scholar
  35. Martin AP, Palumbi SR (1993) Body size, metabolic rate, generation time, and the molecular clock. Proc Natl Acad Sci U S A 90:4087–4091PubMedGoogle Scholar
  36. McCarthy C (1998) Chromas, ver 1.45. Available at:
  37. Menezes G, Rogers A, Krug H, Mendonça A, Stockley BM, Isidro E, Pinho MR, Fernandes A (2001) Seasonal changes in biological and ecological traits of demersal and deep-water fish species in the Azores. Final Report European Commission DGXIV/C/1 Contract 97/081. University of the Azores, Faial, Azores, Portugal, pp 1–162 plus appendicesGoogle Scholar
  38. Milton DA, Shaklee JB (1987) Biochemical genetics and population structure of blue grenadier, Macruronus novaezelandiae (Hector) (Pisces: Merluccidae), from Australian waters. Aust J Mar Freshw Res 38:727–742Google Scholar
  39. Mix AC, Bard E, Schneider R (2001) Environmental processes of the ice age: land, oceans, glaciers (EPILOG). Quatern Sci Rev 20:627–657CrossRefGoogle Scholar
  40. Mulligan TJ, Chapman RW, Brown BL (1992) Mitochondrial DNA analysis of walleye Pollack, Theragra chalcogramma, from the eastern Bering Sea and Shelikof Strait, Gulf of Alaska. Can J Fish Aquat Sci 49:319–326Google Scholar
  41. 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
  42. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  43. Nurminsky DI (2001) Genes in sweeping competition. Cell Mol Life Sci 58:125–134PubMedGoogle Scholar
  44. O’Connell M, Dillon MC, Wright JM, Bentzen P, Merkouris S, Seeb J (1998) Genetic structure among Alaskan Pacific herring populations identified using microsatellite variation. J Fish Biol 53:150–163CrossRefGoogle Scholar
  45. Ostellari L, Bargelloni L, Penzo E, Patarnello P, Patarnello T (1996) Optimization of single-strand conformation polymorphism and sequence analysis of the mitochondrial control region in Pagellus bogaraveo (Sparidae, Teleostei): rationalized tools in fish population biology. Anim Genet 27:423–427PubMedGoogle Scholar
  46. Palumbi SR, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fools guide to PCR, ver 2.0. Kewalo Marine Laboratory, University of Hawaii, HonoluluGoogle Scholar
  47. Pogson GH, Mesa KA, Boutillier RG (1995) Genetic population structure and gene flow in the Atlantic cod Gadus morhua: a comparison of allozyme and nuclear RFLP loci. Genetics 139:375–385PubMedGoogle Scholar
  48. Richardson LR, Gold JR (1997) Mitochondrial DNA diversity in and population structure of the red grouper, Epinephelus morio, from the Gulf of Mexico. Fish Bull 95:174–179Google Scholar
  49. Rogers AD (1994) The biology of seamounts. Adv Mar Biol 30:305–350Google Scholar
  50. Rogers AD (1999) The biology of Lophelia pertusa (Linnaeus 1758) and other deep-water reef-forming corals and impacts from human activities. Int Rev Hydrobiol 84:315–406Google Scholar
  51. Rogers AD (2003) Molecular ecology and evolution of slope species. In: Wefer G, Billett D, Hebbeln D, Jørgensen B, Schlüter M, Weering T van (eds) Ocean margin systems. Springer, Berlin Heidelberg New York, pp 323–337Google Scholar
  52. Ruddiman WF, McIntyre A (1981) The north Atlantic Ocean during the last glaciation. Palaeogeogr Palaeoclimatol Palaeoecol 35:145–214CrossRefGoogle Scholar
  53. Ruzzante DE (1998) A comparison of several measures of genetic distance and population structure with microsatellite data: bias and sampling variance. Can J Fish Aquat Sci 55:1–14Google Scholar
  54. Sambrook J, Fritscher EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  55. Sasaki T (1986) Development and present status of Japanese trawl fisheries in the vicinity of seamounts. In: Uchida RN, Hayasi S, Boehlert GW (eds) Proceedings of the workshop on the environment and resources of seamounts in the North Pacific. U.S. Department of Commerce, NOAA Tech Rep NMFS 43:31–35Google Scholar
  56. Schlötterer C (1998) Microsatellites. In: Hoelzel AR (ed) Molecular genetic analysis of populations: a practical approach, 2nd edn. IRL Press/Oxford University Press, Oxford, pp 237–261Google Scholar
  57. Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis, ver 2.000. Genetics and Biometry Lab, Dept. of Anthropology, University of GenevaGoogle Scholar
  58. 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
  59. Slatkin M (1991) Inbreeding coefficients and coalescence times. Genet Res 58:167–175Google Scholar
  60. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462PubMedGoogle Scholar
  61. Smith PJ, Francis RICC (1982) A glucosephosphate isomerase polymorphism in New Zealand ling Genypterus blacodes. Comp Biochem Physiol 73B:451–455Google Scholar
  62. Spradling TA, Hafner MS, Demastes JW (2001) Differences in the rate of cytochrome-b evolution among species of rodents. J Mammal 82:65–80Google Scholar
  63. Stammatis C, Triantafyllidis A, Moutou A, Mamuris Z (2004) Mitochondrial DNA variation in northeast Atlantic and Mediterranean populations of Norway lobster, Nephrops norvegicus. Mol Ecol 13:1377–1390CrossRefPubMedGoogle Scholar
  64. Stepien CA (1999) Phylogeographic structure of the Dover sole Microstomus pacificus: the larval retention hypothesis and genetic divergence along the deep continental slope of the northeastern Pacific Ocean. Mol Ecol 8:923–939CrossRefPubMedGoogle Scholar
  65. Stockley BM, Rogers AD, Iyengar A, Menezes G, Santos R, Long A (2000) Ten microsatellite loci isolated and developed for the blackspot seabream, Pagellus bogaraveo (Brünnich 1768). Mol Ecol 9:999–1000CrossRefPubMedGoogle Scholar
  66. Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460PubMedGoogle Scholar
  67. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRefPubMedGoogle Scholar
  68. Vis ML, Carr SM, Bowering WR, Davidson WS (1997) Greenland halibut (Reinhardtius hippoglossoides) in the North Atlantic are genetically homogenous. Can J Fish Aquat Sci 54:1813–1821CrossRefGoogle Scholar
  69. Waldman JR, Bender RE, Wirgin II (1998) Multiple population bottlenecks and DNA diversity in populations of wild striped bass, Morone saxatilis. Fish Bull 96:614–620Google Scholar
  70. Ward RD, Elliot NG, Grewe PM, Last PR, Lowry PS, Innes BH, Yearsley GK (1998) Allozyme and mitochondrial DNA variation in three species of oreos (Teleostei: Oreosomatidae) from Australian waters. N Z J Mar Freshw Res 32:233–245Google Scholar
  71. Weber DS, Stewart BS, Garza JC, Lehman N (2000) An empirical genetic assessment of the severity of the northern elephant seal population bottleneck. Curr Biol 10:1287–1290CrossRefPubMedGoogle Scholar
  72. Whitlock M, McCauley D (1999) Indirect measures of gene flow and migration: FST doesn’t equal 1/(4Nm+1). Heredity 82:117–125CrossRefPubMedGoogle Scholar
  73. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159Google Scholar
  74. Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • B. Stockley
    • 1
  • G. Menezes
    • 2
  • M. R. Pinho
    • 2
  • A. D. Rogers
    • 3
  1. 1.School of Ocean & Earth ScienceUniversity of Southampton, Southampton Oceanography CentreSouthamptonUK
  2. 2.Departamento de Oceanografia e Pescas da Universidade dos Açores Horta, AçoresPortugal
  3. 3.British Antarctic SurveyNatural Environment Research CouncilCambridgeUK

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