Marine Biology

, Volume 153, Issue 1, pp 47–60

Population genetic structure of the stalked barnacle Pollicipes pollicipes (Gmelin, 1789) in the northeastern Atlantic: influence of coastal currents and mesoscale hydrographic structures

  • J. Quinteiro
  • J. Rodríguez-Castro
  • M. Rey-Méndez
Research Article
  • 259 Downloads

Abstract

Within its distribution range in the northeastern Atlantic, the stalked barnacle Pollicipes pollicipes shows a well-defined pattern of genetic variation, comprising (a) a subtropical/temperate northern assemblage, made up of populations distributed between 47°N and 28°N along the French, Iberian, North African and Canary Islands coastlines, and (b) a single isolated and highly divergent tropical population in the Cape Verde Islands (16°N), at the southernmost limit of the species’ distribution. However, within the northern assemblage several populations show a level of genetic differentiation that allows rejection of the hypothesis of genetic homogeneity. The congruence observed between genetic and hydrographic patterns suggests a crucial role of hydrodynamics, and of the dispersal of the planktonic larvae, in the determination of population structure. Along the southern European Atlantic coast, the Iberian Poleward Current and mesoscale hydrographic structures are, respectively, facilitating gene flow at the regional level and genetic differentiation at the local level. On the Atlantic coast of North Africa, the homogenizing equatorward flow of the Canary Current does not extend as far as the Cape Verde Islands. A demographic expansion is dated to the late Pleistocene, preceding the Eemian interglacial, and is oldest in the case of the long-standing Cape Verde population, sustained by a stable tropical habitat. The divergence between the Cape Verde population and the remaining populations is thus ancient, and suggests that oceanic current patterns may constitute a generalized physical barrier to the dispersal of marine organisms between Cape Verde and the rest of Macaronesia.

References

  1. Abelson A, Denny M (1997) Settlement of marine organisms in flow. Annu Rev Ecol Syst 28:317–339CrossRefGoogle Scholar
  2. 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 14:1343–1354PubMedCrossRefGoogle Scholar
  3. Aris-Brosou S, Excoffier L (1996) The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Mol Biol Evol 13:494–504PubMedGoogle Scholar
  4. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  5. Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedGoogle Scholar
  6. Barber PH, Palumbi SR, Erdmann MV, Moosa K (2002) Sharp genetic breaks among populations of Haptosquilla pulchella (Stomatopoda) indicate limits to larval transport: patterns, causes, and consequences. Mol Ecol 11:659–674PubMedCrossRefGoogle Scholar
  7. Barnes M (1992) The reproductive periods and condition of the penis in several species of common cirripedes. Oceanogr Mar Biol 30:483–525Google Scholar
  8. Barnes M (1996) Pedunculate cirripedes of the genus Pollicipes. Oceanogr Mar Biol 34:303–394Google Scholar
  9. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568PubMedCrossRefGoogle Scholar
  10. Bertness MD, Gaines SD (1993) Larval dispersal and local adaptation in acorn barnacles. Evolution 47:316–320CrossRefGoogle Scholar
  11. Bilodeau AL, Felder DL, Neigel JE (2005) Population structure at two geographic scales in the burrowing crustacean Callichirus islagrande (Decapoda, Thalassinidea): historical and contemporary barriers to planktonic dispersal. Evolution 59:2125–2138PubMedGoogle Scholar
  12. Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45PubMedCrossRefGoogle Scholar
  13. Bory A, Jeandel C, Leblond N, Vangriesheim A, Khriponoff A, Beaufort L, Rabouille C, Nicolas E, Tachikawa K, Etcheber H (2001) Downward particle fluxes within different productivity regimes off the Mauritanian upwelling zone (EUMELI program). Deep Sea Res I 48:2251–2282CrossRefGoogle Scholar
  14. Briggs JC (1995) Global biogeography. Elsevier, AmsterdamCrossRefGoogle Scholar
  15. Brown AF, Kann LM, Rand DM (2001) Gene flow versus local adaptation in the northern acorn barnacle, Semibalanus balanoides: insights form mitochondrial DNA variation. Evolution 55:1972–1979PubMedGoogle Scholar
  16. Bucklin A, Wiebe PH (1998) Low mitochondrial diversity and small effective population sizes of the copepods Calanus finmarchicus and Nannocalanus minor: possible impact of climatic variation during recent glaciation. J Hered 89:383–392PubMedCrossRefGoogle Scholar
  17. Butman CA (1987) Larval settlement of soft-sediment invertebrates: the spatial scales of pattern explained by active habitat selection and the emerging role of hydrodynamical processes. Oceanogr Mar Biol Ann Rev 25:113–165Google Scholar
  18. Caley MJ, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA (2005) Recruitment and the local dynamics of the open marine populations. Annu Rev Ecol Syst 27:477–500CrossRefGoogle Scholar
  19. Cardoso AC, Yule AB (1995) Aspects of the reproductive biology of Pollicipes pollicipes (Cirripedia; Lepadomorpha) from the southwest coast of Portugal. Neth J Aquat Ecol 29:391–396CrossRefGoogle Scholar
  20. Cruz T (1993) Growth of Pollicipes pollicipes (Gmelin, 1970) (Cirripedia, Lepadomorha) on the SW coast of Portugal. Crustaceana 65:151–158CrossRefGoogle Scholar
  21. Cruz T (2000) Biologia e ecologia do percebe Pollicipes pollicipes (Gmelin, 1790) no litoral sudoeste português. Dr in Marine Biology Universidade de ÉvoraGoogle Scholar
  22. Cruz T, Hawkins SJ (1998) Reproductive cycle of Pollicipes pollicipes at Cabo de Sines, south-west coast of Portugal. J Mar Biol Assoc UK 78:483–496Google Scholar
  23. De la Hoz JJ, García L (1993) Datos para el estudio de la distribución y reproducción del percebe, Pollicipes cornucopia (Leach), en Asturias. Publ Espec Inst Esp Oceanogr 11:65–70Google Scholar
  24. Duran S, Palcin C, Becerro MA, Turon X, Giribet G (2004) Genetic diversity and population structure of the commercially harvested sea urchin Paracentrotus lividus (Echinodermata, Echinoidea). Mol Ecol 13:3317–3328PubMedCrossRefGoogle Scholar
  25. 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 131:479–491PubMedGoogle Scholar
  26. 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
  27. Fedoseev A (1970) Geostrophic circulation of surface waters on the shelf of north-west Africa. Rapp P-V Reun Cons Int Explor Mer 159:165–175Google Scholar
  28. Freire J, García-Allut A (2000) Socioeconomical and biological causes of management failures in European artisanal fisheries: the case of Galicia (NW Spain). Mar Pol 24:375–384CrossRefGoogle Scholar
  29. Frouin R, Fuiza AF, Ambar I, Boyd TJ (1990) Observations of a poleward surface current off the coasts of Portugal and Spain during the winter. J Geophys Res 95:679–691Google Scholar
  30. Fu Y-X (1997) Statistical tests of neutrality against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  31. Gil J (1995) Inestabilidades, fenómenos de mesoescala y movimiento vertical a lo largo del borde sur del golfo de Vizcaya. Bol Inst Esp Oceanogr 11:141–159Google Scholar
  32. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  33. Hanski I, Simberloff D (1997) The metapopulation approach, its history, conceptual domain, and application to conservation. In: Hanski I, Gilpin ME (eds) Metapopulation biology: ecology, genetics and evolution. Academic, San DiegoGoogle Scholar
  34. Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600PubMedGoogle Scholar
  35. Hawkins SJ, Corte-Real HBSM, Pannacciulli FG, Weber LC, Bishop JDD (2000) Thoughts on the ecology and evolution of the intertidal biota of the Azores and other Atlantic islands. Hydrobiologia 440:3–17CrossRefGoogle Scholar
  36. Haynes R, Barton ED (1990) A poleward flow along the Atlantic coast of the Iberian Peninsula. J Geophys Res 95:11425–11441Google Scholar
  37. Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913PubMedCrossRefGoogle Scholar
  38. Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011–2014PubMedGoogle Scholar
  39. Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132:583–589PubMedGoogle Scholar
  40. Hyder K, Aberg P, Johnson MP, Hawkins SJ (2001) Models of open populations with space-limited recruitment: extension of theory and application to the barnacle Chthamalus montagui. J Anim Ecol 70:853–863CrossRefGoogle Scholar
  41. Jolly MT, Jollivet D, Gentil F, Thiébaut E, Viard F (2005) Sharp genetic break between Atlantic and English Channel populations of the polychaete Pectinaria koreni, along the North coast of France. Heredity 94:23–32PubMedCrossRefGoogle Scholar
  42. Karlson RH, Levitan DR (1990) Recruitment-limitation in open populations of Diadema antillarum: an evaluation. Oecologia 82:40–44CrossRefGoogle Scholar
  43. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRefGoogle Scholar
  44. Knoll M, Henández-Guerra A, Lenz B, López Laatzen F, Machín F, Müller TJ, Siedler G (2002) The eastern boundary current system between the Canary Islands and the African Coast. Deep-Sea Res II 49:3427–3440CrossRefGoogle Scholar
  45. Koutsikopoulos C, Le Cann B (1996) Physical processes and hydrological structures related to the Bay of Biscay anchovy. Sci Mar 60:9–19Google Scholar
  46. Lauzier RB (1999) Framework for goose barnacle (Pollicipes polymerus Sowerby, 1833) fishery in waters off the West Coast of Canada. 99/198. Canadian Stock Assessment Secretariat. Research DocumentGoogle Scholar
  47. Lewis CA (1975) Development of the gooseneck barnacle Pollicipes polymerus (Cirripedia: Lepadomorpha): fertilization through settlement. Mar Biol 32:141–153CrossRefGoogle Scholar
  48. Martins CS, Hamann M, Fiúza AFG (2002) Surface circulation in the eastern North Atlantic, from drifters and altimetry. J Geophys Res 107:1–15CrossRefGoogle Scholar
  49. McElroy D, Moran P, Bermingham E, Kornfield I (1992) REAP: an integrated environment for the manipulation and phylogenetic analysis of restriction data. J Hered 83:157–158PubMedGoogle Scholar
  50. Mittelstaedt E (1991) The ocean boundary along the northwest African coast: circulation and oceanographic properties at the sea surface. Prog Oceanogr 26:307–355CrossRefGoogle Scholar
  51. Molares J (1993) Estudio del ciclo biológico del percebe (Pollicipes cornucopia Leach) de las costas de Galicia. Alimentaria 248:9–71Google Scholar
  52. Molares J, Freire J (2003) Development and perspectives for community-based management of the goose barnacle (Pollicipes pollicipes) fisheries in Galicia (NW Spain). Fish Res 65:485–492CrossRefGoogle Scholar
  53. Molares J, Tilves F, Quintana R, Rodríguez S, Pascual C (1994) Gametogenesis of Pollicipes cornucopia (Cirripedia: Scalpellomorpha) in north-west Spain. Mar Biol 120:553–560CrossRefGoogle Scholar
  54. Monteiro FA, Solé-Cava AM, Thorpe JP (1997) Extensive genetic divergence between populations of the common intertidal sea anemone Actinia equina from Britain, the Mediterranean and the Cape Verde Islands. Mar Biol 129:425–433CrossRefGoogle Scholar
  55. Moritz C (1994) Defining "evolutionary significant units" for conservation. Trends Ecol Evol 9:373CrossRefGoogle Scholar
  56. O’Riordan RM, Arenas F, Arrontes J, Castro JJ, Cruz T, Delany J, Martínez B, Fernandez C, Hawkins SJ, McGrath D, Myers AA, Oliveros J, Pannacciulli FG, Power AM, Relini G, Rico JM, Silva T (2004) Spatial variation in the recruitment of the intertidal barnacles Chthamalus montagui Southward and Chthamalus stellatus (Poli) (Crustacea: Cirripedia) over an European scale. J Exp Mar Biol Ecol 304:243–264CrossRefGoogle Scholar
  57. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  58. Pannacciulli FG, Bishop JDD, Hawkins SJ (1997) Genetic structure of populations of two species of Chthamalus (Crustacea: Cirripedia) in the north-east Atlantic and Mediterranean. Mar Biol 128:73–82CrossRefGoogle Scholar
  59. Pingree RD, Le Cann B (1989) Celtic and Armorican slope and shelf residual currents. Prog Oceanogr 23:303–338CrossRefGoogle Scholar
  60. Quesada H, Beynon CM, Skibinski DAG (1995) A mitochondrial DNA discontinuity in the mussel Mytilus galloprovincialis Lmk: Pleistocene vicariance biogeography and secondary interdegradation. Mol Biol Evol 12:521–524PubMedGoogle Scholar
  61. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100PubMedGoogle Scholar
  62. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283CrossRefGoogle Scholar
  63. Robinson SG, Maslin MA, McCave IN (1995) Magnetic susceptibility variations in upper Pleistocene deep-sea sediments of the NE Atlantic: implications for ice rafting and paleocirculation at the last glacial maximum. Paleoceanography 10:221–250CrossRefGoogle Scholar
  64. Roff DA, Bentzen P (1989) The statistical analysis of mitochondrial DNA polymorphisms: χ2 and the problem of small samples. Mol Biol Evol 6:539–545PubMedGoogle Scholar
  65. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  66. Roughgarden J, Iwasa Y, Baxter C (1985) Demographic theory for an open marine population with space-limited recruitment. Ecology 66:54–67CrossRefGoogle Scholar
  67. Rozas J, Sánchez-del Barrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  68. Salomon JC, Breton M (1993) An atlas of long term currents in the channel. Oceanol Act 16:439–448Google Scholar
  69. Sánchez F, Gil J (2000) Hydrographic mesoscale structures and poleward current as a determinant of hake (Merluccius merluccius) recruitment in southern Bay of Biscay. ICES J Mar Sci 57:170Google Scholar
  70. Schmidt PS, Rand DM (2001) Adaptative maintenance of genetic polymorphism in an intertidal barnacle: habitat- and life-stage-specific survivorship of Mpi genotypes. Evolution 55:1336–1344PubMedGoogle Scholar
  71. 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 152:1079–1089PubMedGoogle Scholar
  72. Sotka EE, Wares JP, Barth JA, Grosberg RK, Palumbi SR (2004) Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula. Mol Ecol 13:2143–2156PubMedCrossRefGoogle Scholar
  73. Stamatis C, Triantafyllidis A, Moutou KA, Mamuris Z (2004) Mitochondrial DNA variation in northeast Atlantic and Mediterranean populations of Norway lobster, Nephrops norvergicus. Mol Ecol 13:1377–1390PubMedCrossRefGoogle Scholar
  74. Swofford DL (2002) PAUP* Phylogenetic analysis using parsimony (* and other methods) (4.0b10). Sinauer Associates, SunderlandGoogle Scholar
  75. Tajima F (1989a) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  76. Tajima F (1989b) The effect of change in population size on DNA polymorphism. Genetics 123:597–601PubMedGoogle Scholar
  77. 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 10:512–526PubMedGoogle Scholar
  78. Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribean reef fish. Science 299:107–109PubMedCrossRefGoogle Scholar
  79. Thunnell RC (1979) Eastern Mediterranean Sea during the last glacial maximum; an 18,000-years B.P. reconstruction. Quatern Res 11:353–372CrossRefGoogle Scholar
  80. Vangriesheim A, Boutnot-Marec C, Fontan AC (2003) Flow variability near the Cape Verde frontal zone (subtropical Atlantic Ocean). Oceanol Act 26:149–159CrossRefGoogle Scholar
  81. Varela RA, Rosón G, Herrera JL, Torres-López S, Fernández-Romero A (2005) A general view of the hydrographic and dynamical patterns of the Rías Baixas adjacent sea area. J Mar Syst 54:97–113CrossRefGoogle Scholar
  82. Wares JP (2001) Patterns of speciation inferred form mitochondrial DNA in North American Chthmalus (Cirripedia: Balanomorpha: Chthmaloidea). Mol Phyl Evol 18:104–116CrossRefGoogle Scholar
  83. Wares JP, Gaines SD, Cunningham CW (2001) A comparative study of asymmetric migration events across a marine biogeographic boundary. Evolution 55:295–306PubMedGoogle Scholar
  84. Zane L, Ostellari L, Maccatrozzo L, Bargelloni L, Cuzin-Roudy J, Buchholz F, Patarnello T (2000) Genetic differentiation in a pelagic crustacean (Meganyctiphanes norvegica: Euphausiacea) from the North East Atlantic and the Mediterranean Sea. Mar Biol 136:191–199CrossRefGoogle Scholar
  85. Zhou M, Paduan JD, Niiler PP (2000) Surface currents in the Canary Basin from drifter observations. J Geophys Res 105:21893–21911CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • J. Quinteiro
    • 1
  • J. Rodríguez-Castro
    • 1
  • M. Rey-Méndez
    • 1
  1. 1.Departamento de Bioquímica e Bioloxía Molecular, Facultade de BioloxíaSantiago de CompostelaGalicia, Spain

Personalised recommendations