Skip to main content

Advertisement

Log in

Phylogeography of the European stalked barnacle (Pollicipes pollicipes): identification of glacial refugia

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The alternation of glacial and interglacial events during the Pleistocene has produced changes in species distribution ranges leading to bottlenecks and alterations of patterns of gene flow. The European stalked barnacle, Pollicipes pollicipes, is a sessile pedunculate cirripede that inhabits the rocky intertidal frame, from Senegal to the northwestern coast of France. In this work, we have analyzed a fragment of the mitochondrial gene cytochrome c oxidase subunit I for 569 individuals of P. pollicipes in order to investigate whether the shifts in climatic conditions that occurred during the Pleistocene influenced the current pattern of distribution of genetic variation of P. pollicipes. A pre-last glacial maximum pattern of demographic expansion was found, in concordance with many other North Atlantic marine species. On the other hand, three potential glacial refugia were identified: North African coasts, northwestern Iberian Peninsula and English Channel/Brittany.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell, Malden

    Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Barnes M (1996) Pedunculate cirripedes of the genus Pollicipes. Oceanogr Mar Biol Annu Rev 34:303–394

    Google Scholar 

  • Barnes M, Barnes H (1962) The distribution and general ecology of Balanus balanoides together with some observations on Balanus improvisus in the waters around the coasts of Denmark, southern Sweden and northeast Germany. Lund Universitets Arskrift N.F. AVD, vol 58

  • Chevolot M, Hoarau G, Rijnsdorp AD, Stam WT, Olsen JL (2006) Phylogeography and population structure of thornback rays (Raja clavata L., Rajidae). Mol Ecol 15:3693–3705

    Article  CAS  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  PubMed  Google Scholar 

  • Coyer JA, Diekmann O, Serrão EA, Procaccini G, Milchakova N, Pearson GA et al (2004) Population genetics of dwarf eelgrass Zostera noltii throughout its biogeographic range. Mar Ecol-Prog Ser 281:51–62

    Article  Google Scholar 

  • Crisp DJ, Bourget E (1985) Growth in barncales. Adv Mar Biol 22:199–244

    Article  Google Scholar 

  • Cruz T (1993) Growth of Pollicipes pollicipes (Gmelin, 1970) (Cirripedia, Lepadomorpha) on the SW coast of Portugal. Crustaceana 65:151–158

    Article  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: bayesian evolutionary analysis sampling trees. BMC Evol Biol 7:214

    Article  PubMed  PubMed Central  Google Scholar 

  • Duran S, Palacín 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(11):3317–3328

    Article  CAS  PubMed  Google Scholar 

  • Estoup A, Largiadèr CR, Perrot E, Chourrout D (1996) Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic marker and transgenes. Mol Mar Biol Biotechnol 5(4):295–298

    CAS  Google Scholar 

  • 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 131:479–491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    Article  CAS  Google Scholar 

  • Fu YX (1997) Statistical test of neutrality of mutations against population growth, hitch-hiking and biological selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garrick RC, Dyer RJ, Beheregaray LB, Sunnucks P (2008) Babies and bathwater: a comment on the premature obituary for nested clade phylogeographical analysis. Mol Ecol 17:1401–1403

    Article  CAS  PubMed  Google Scholar 

  • Gómez A, Hughes RN, Wright PJ, Carvalho GR, Lunt DH (2007) Mitochondrial DNA phylogeography and mating compatibility reveal marked genetic structuring and speciation in the NE Atlantic bryozoan Celleporella hyalina. Mol Ecol 16:2173–2188

    Article  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hartl DL, Clark AG (1997) Principles of population genetics. Sinauer, Sunderland, MA

    Google Scholar 

  • Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc Lond 58:247–276

    Article  Google Scholar 

  • Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Phil Trans R Soc B 359:183–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoarau G, Coyer JA, Veldsink JH, Stam WT, Olsen JL (2007) Glacial refugia and recolonization pathways in the brown seaweed Fucus serratus. Mol Ecol 16:3606–3616

    Article  CAS  PubMed  Google Scholar 

  • Jolly MT, Viard F, Gentil F, Thiébaut E, Jollivet D (2006) Comparative phylogeography of two coastal polychaete tubeworms in the Northeast Atlantic supports shared history and vicariant events. Mol Ecol 15:1841–1855

    Article  CAS  PubMed  Google Scholar 

  • Kellaway GA, Redding HH, Shephard-Thorn ER, Destombes JP (1975) The quaternary history of the English Channel. Phil Trans R Soc A 279:189–218

    Article  Google Scholar 

  • Luttikhuizen PC, Drent J, Baker AJ (2003) Disjunct distribution of highly diverged mitochondrial lineage clade and population subdivision in a marine bivalve with pelagic larval dispersal. Mol Ecol 12:2215–2229

    Article  CAS  PubMed  Google Scholar 

  • Marko PB (2004) ‘What’s larvae got to do with it?’ Contrasting patterns of postglacial population structure in two benthic marine gastropods with identical larval dispersal capabilities. Mol Ecol 13:597–611

    Article  CAS  PubMed  Google Scholar 

  • McDonald J, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654

    Article  CAS  PubMed  Google Scholar 

  • Molares J (1993) Estudio del ciclo biológico del percebe (Pollicipes cornucopia Leach) de las costas de Galicia. Alimentaria 248:9–71

    Google Scholar 

  • Molares J, Tilves F, Quintana R, Rodríguez S, Pascual C (1994) Gametogenesis of Pollicipes cornucopia (Cirripedia: Scalpellomorpha) in north-west Spain. Mar Biol 120:553–560

    Article  Google Scholar 

  • Olsen JL, Stam WT, Coyer JA, Reusch TBH, Billingham M, Boström C et al (2004) North Atlantic phylogeography and large-scale population differentiation of the seagrass Zoostera marina L. Mol Ecol 13:1923–1941

    Article  CAS  PubMed  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Cons Biol 12:844–855

    Article  Google Scholar 

  • Pfenninger M, Posada D (2002) Phylogeographic history of the land snail Candidula unifasciata (Helicellinae, Stylommatophora): fragmentation, corridor migration, and secondary contact. Evolution 56(9):1776–1788

    Article  PubMed  Google Scholar 

  • Posada D, Crandall K (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Posada D, Crandall K, Templeton AR (2000) GEODIS: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol Ecol 9:487–488

    Article  CAS  PubMed  Google Scholar 

  • Provan J, Bennett KD (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23(10):564–571

    Article  PubMed  Google Scholar 

  • Provan J, Wattier RA, Maggs CA (2005) Phylogeographic analysis of the red seaweed Palmaria palmata reveals a Pleistocene marine glacial refugium in the English Channel. Mol Ecol 14:793–804

    Article  CAS  PubMed  Google Scholar 

  • Quinteiro J, Rodríguez-Castro J, Rey-Méndez M (2007) Population genetic structure of the stalked barnacle Pollicipes pollicipes (Gmelin, 1789) in the northeastern Atlantic: influence of coastal currents and mesoscale hydrographic structures. Mar Biol 153:47–60

    Article  Google Scholar 

  • Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality test against population growth. Mol Biol Evol 19(1):2092–2100

    Article  CAS  PubMed  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • 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(6):1377–1390

    Article  CAS  PubMed  Google Scholar 

  • Svendsen JI, Alexanderson H, Astakhov VI et al (2004) Late Quaternary ice sheet history of northern Eurasia. Quat Sci Rev 23:1229–1271

    Article  Google Scholar 

  • Tajima F (1993) Simple methods for testing molecular clock hypothesis. Genetics 135:599–607

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 10:512–526

    CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Templeton A (2001) Using phylogeographic analyses of gene trees to test species status and processes. Mol Ecol 10:779–791

    Article  CAS  PubMed  Google Scholar 

  • Templeton A, Boerwinkle E, Sing CF (1987) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of Alcohol Dehydrogenase activity in Drosophila. Genetics 117:343–351

    CAS  PubMed  PubMed Central  Google Scholar 

  • Templeton A, Crandall KA, Sing C (1992) A cladistic-analysis of phenotypic associations with haplotypes inferred from restriction endonucleases mapping and DNA-sequence data. Genetics 132:619–633

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Syoc RJ (1994) Genetic divergence between subpopulations of the eastern Pacific goose barnacle Pollicipes elegans: mitochondrial cytochrome c subunit 1 nucleotide sequences. Mol Mar Biol Biotechnol 3(6):338–346

    PubMed  Google Scholar 

  • Van Syoc RJ (1995) Barnacle mitochondrial DNA: determining genetic relationship among species of Pollicipes. In: Schram FR, Høeg JT (eds) New frontiers in barnacle evolution. Crustacean Issues, Rotterdam, pp 269–296

    Google Scholar 

  • Wares JP (2001) Patterns of speciation inferred from mitochondrial DNA in North American Chthmalus (Cirripedia: Balanomorpha: Chthmaloidea). Mol Phylogenet Evol 18:104–116

    Article  CAS  PubMed  Google Scholar 

  • Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55(12):2455–2469

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Samples were collected with the help of Ramón Riveiro, Jorge L. Alcázar and other anonymous collaborators. We want to thank Dr. Galice Hoarau for precious help in focusing the paper. Dr. David Posada helped us with the NCA. Prof. Francis Juanes revised the article and corrected the English. We also want to thank two anonymous reviewers for helpful comments. This study has been financially supported by the Xunta de Galicia (Spain), Grant SV-05-XUNTA-1.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel Campo.

Additional information

Communicated by M. I. Taylor.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(PDF 43 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Campo, D., Molares, J., Garcia, L. et al. Phylogeography of the European stalked barnacle (Pollicipes pollicipes): identification of glacial refugia. Mar Biol 157, 147–156 (2010). https://doi.org/10.1007/s00227-009-1305-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-009-1305-z

Keywords

Navigation