Skip to main content
SpringerLink
Log in

Meso-scale hydrodynamic and reproductive asynchrony affects the source–sink metapopulation structure of the coastal polychaete Pectinaria koreni

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

Abstract

The polychaete Pectinaria koreni exhibits a complex life cycle characterized by non-overlapping generations and widespread larval dispersal. To explore how “local” metapopulation genetic structure varies spatially and temporally during population turnover, we combined observations on demography, larval dispersal through hydrodynamic modelling and population genetics of successive age cohorts in the Baie de Seine (eastern English Channel, France). Mature adults (March), newly settled (July) and later-stage juveniles (September) were sampled in 2003 on the edge and in the main demes of the metapopulation. Demes displayed an asynchronous dynamics due to variations in habitat quality affecting reproductive timing (e.g. three distinct spawning events observed) and in local larval supply linked to temporal fluctuations of hydrodynamism. Two-source populations were identified among dense areas with the greatest larval retention and self-recruitment rates: one with a single recruitment event, stable temporal genetic variation and a strong spatial genetic re-homogenization during turnover, and the other with two recruitment events and significant allele frequency changes over time. Sink habitats displayed single recruitment event and experienced strong inter-generational (juveniles vs adults) genetic changes due to genetic drift associated with strong winter mortalities. Altogether, results suggested that adult spawning asynchrony and sweepstakes reproductive success, together with genetic drift, played a greater role than hydrodynamics itself in determining effective recruitment rates at some sites and generating genetic patchiness.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Bailly du Bois P, Dumas F (2005) Fast hydrodynamic model for medium- and long-term dispersion in seawater in the English Channel and southern North Sea, qualitative and quantitative validation by radionuclide tracers. Ocean Model 9:169–210

    Article  Google Scholar 

  • Barnay AS (2003) Structure des peuplements de sables fins plus ou moins envasés en Manche: échelles spatiales et biodiversité. Dissertation, University Pierre & Marie Curie

  • Battacharya CG (1967) A simple method of resolution of a distribution into Gaussian components. Biometrics 23:115–135

    Article  Google Scholar 

  • Belkhir K, Borsa P, Goudet J, Chikhi L, Bonhomme F (2002) GENETIX 4.03, logiciel sous Windows TM pour la génétique des populations. Université de Montpellier 2, Montpellier

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  • Breton M, Salomon JC (1995) A 2D long-term advection-dispersion model for the Channel and southern North Sea. Part A: validation through comparison with artificial radionuclides. J Mar Syst 6:495–514

    Article  Google Scholar 

  • Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5:4534–4555

    Google Scholar 

  • Broquet T, Viard F, Yearsley JM (2012) Genetic drift and collective dispersal can result in chaotic genetic patchiness. Evolution 67:1660–1675

    Article  Google Scholar 

  • Chao A, Shen T-J (2010) Program SPADE (species prediction and diversity estimation). Program and User’s Guide, http://chao.stat.nthu.edu.tw

  • Dauvin JC, Thiébaut E, Geisteira JLG, Ghertsos K, Gentil F, Ropert M, Sylvand B (2004) Spatial structure of a subtidal macrobenthic community in the Bay of Veys (western Bay of Seine, English Channel). J Exp Mar Biol Ecol 307:217–235

    Article  Google Scholar 

  • David P, Perdieu M-A, Pernot A-F, Jarne P (1997) Fine-grained spatial and temporal population genetic structure in the marine bivalve Spisula ovalis. Evolution 51:1318–1322

    Article  Google Scholar 

  • Doncaster CP, Clobert J, Doligez B, Gustafsson L, Danchin E (1997) Balanced dispersal between spatially varying local populations: an alternative to the source-sink model. Am Nat 150:425–445

    Article  CAS  Google Scholar 

  • Dubois S, Comtet T, Retière C, Thiébaut E (2007) Distribution and retention of Sabellaria alveolata larvae (Polychaeta: Sabellariidae) in the Bay of Mont-Saint-Michel, France. Mar Ecol Prog Ser 346:243–254

    Article  CAS  Google Scholar 

  • Eldon B, Wakeley J (2009) Coalescence times and F ST under a skewed offspring distribution among individuals in a population. Genetics 181:615–629

    Article  Google Scholar 

  • Elkaïm B, Irlinger JP (1987) Contribution à l’étude de la dynamique des populations de Pectinaria koreni Malgrem (Polychète) en Baie de Seine orientale. J Exp Mar Biol Ecol 107:171–197

    Article  Google Scholar 

  • Ellien C, Thiébaut E, Barnay AS, Dauvin JC, Gentil F, Salomon JC (2000) The influence of variability in larval dispersal on the dynamics of a marine metapopulation in the eastern Channel. Oceanol Acta 23:423–442

    Article  Google Scholar 

  • Ellien C, Thiébaut E, Dumas F, Salomon JC, Nival P (2004) Modelling approach of the respective role of hydrodynamic processes on larval dispersal and of larval mortality on the recruitment of benthic invertebrates: example of Pectinaria koreni in the Bay of Seine. J Plankton Res 26:117–132

    Article  Google Scholar 

  • Gaggiotti OE (1996) Population genetic models of source-sink metapopulations. Theor Popul Biol 50:178–208

    Article  Google Scholar 

  • Gaggiotti OE, Smouse PE (1996) Stochastic migration and maintenance of genetic variation in sink populations. Am Nat 147:919–945

    Article  Google Scholar 

  • Gayanilo FC, Sparre P, Pauly D (2005) FAO-ICLARM stock assessment tools II (FiSAT II version 1.2.2). FAO Computerized Information Series 8 (Fisheries), Rome

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Hanski I (1999) Metapopulation ecology. Oxford University Press, New York

    Google Scholar 

  • Harrison S, Hastings A (1996) Genetic and evolutionary consequences of metapopulation structure. Trends Ecol Evol 11:180–183

    Article  CAS  Google Scholar 

  • Hastings A, Harrison S (1994) Metapopulation dynamics and genetics. Ann Rev Ecol Syst 25:167–188

    Article  Google Scholar 

  • Hedgecock D (1994) Does variance in reproductive success limit effective population sizes of marine organisms? In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapman & Hall, London, pp 122–134

    Google Scholar 

  • Hedgecock D, Pudovkin AI (2011) Sweepstakes reproductive success in highly fecund marine fish and shellfish: a review and commentary. Bull Mar Sci 87:971–1002

    Article  Google Scholar 

  • Hendry AP, Troy D (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Mol Ecol 14:901–916

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Irlinger JP, Gentil F, Quintino V (1991) Reproductive biology of the polychaete Pectinaria koreni (Malmgren) in the Bay of Seine (English channel). Ophelia Suppl 5:343–350

    Google Scholar 

  • James MK, Armsworth PR, Mason LB, Bode L (2002) The structure of reef fish metapopulations: modelling larval dispersal and retention patterns. Proc R Soc Lond B 269:2079–2086

    Article  Google Scholar 

  • Johnson MS, Black R (1984) Pattern beneath the chaos: the effect of recruitment on genetic patchiness in an intertidal limpet. Evolution 38:1371–1383

    Article  Google Scholar 

  • Johnson MS, Holborn K, Black R (1993) Fine-scale patchiness and genetic heterogeneity of recruits of the corallivorous gastropod Drupella cornus. Mar Biol 117:91–96

    Article  Google Scholar 

  • Jolly MT, Viard F, Weinmayr G, Gentil F, Thiébaut E, Jollivet D (2003) Does the genetic structure of Pectinaria koreni (Polychaeta: Pectinariidae) conform to a source-sink metapopulation model at the scale of the Baie de Seine? Helgoland Mar Res 56:238–246

    Google Scholar 

  • 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 94:23–32

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jolly MT, Ellien C, Gentil F, Guyard P, Viard F, Thiébaut E, Jollivet D (2009) Population genetics and hydrodynamic modelling of larval dispersal dissociate contemporary patterns of connectivity from historical expansion into European shelf seas in the polychaete Pectinaria koreni (Malmgren). Limnol Oceanogr 54:2089–2106

    Article  Google Scholar 

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  Google Scholar 

  • Jost L (2009) D vs. GST: response to Heller and Siegismund (2009) and Ryman and Leimar (2009). Mol Ecol 18:2088–2091

  • Lagadeuc Y (1992) Transport larvaire en Manche. Exemple de Pectinaria koreni (Malmgren), annélide polychète, en baie de Seine. Oceanol Acta 15:383–395

    Google Scholar 

  • Lagadeuc Y, Retière C (1993) Critères d’identification rapide des stades de développement des larves de Pectinaria koreni (Malmgren) (Annélide Polychète) de la Baie de Seine (Manche). Vie et Milieu 43:217–224

    Google Scholar 

  • Lambert R (1991) Recrutement d’espèces benthiques à larves planctoniques en régime mégatidal. Cas de Pectinaria koreni (Malmgren), annélide polychète. Dissertation, University of Rennes I

  • Lambert R, Lagadeuc Y, Retière C (1996) Metamorphosis of Pectinaria koreni (Annelida: Polychaeta) and recruitment of an isolated population in the English Channel. J Mar Biol Assoc UK 76:23–36

    Article  Google Scholar 

  • Lewis RI, Thorpe JP (1994) Temporal stability of gene frequencies within genetically heterogeneous populations of the queen scallop Aequipecten (Chlamys) opercularis. Mar Biol 121:117–126

    Article  Google Scholar 

  • McCauley DE (1991) Genetic consequences of local extinction and recolonization. Trends Ecol Evol 6:5–8

    Article  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326

    Article  CAS  Google Scholar 

  • Muths D, Jollivet D, Gentil F, Davoult D (2009) Large-scale genetic patchiness among NE Atlantic populations of the brittle star Ophiothrix fragilis. Aquat Biol 5:117–132

    Article  Google Scholar 

  • Muths D, Davoult D, Jolly MT, Gentil F, Jollivet D (2010) Pre-zygotic factors best explain reproductive isolation between hybridizing species of brittle-stars Acrocnida brachiata and A. spatulispina (Echinodermata: Ophiuroidea). Genetica 138:667–679

    Article  CAS  Google Scholar 

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323

    Article  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nicolaidou A (1983) Life history and productivity of Pectinaria koreni Malmgren (Polychaeta). Estuar Coast Shelf Sci 17:31–43

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetic software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rumrill SS (1990) Natural mortality of marine invertebrate larvae. Ophelia 32:163–198

    Article  Google Scholar 

  • Salomon JC, Guéguéniat P, Orbi A, Baron Y (1988) A Lagrangian model for long-term tidally-induced transport and mixing. Verification by artificial radionuclide concentrations. In: Guary JC, Guéguéniat P, Pentreath RJ (eds) Radionuclides: a tool for Oceanography. Elsevier Applied Science Publishers, London, pp 384–394

    Google Scholar 

  • Selkoe KA, Gaines SD, Caselle JE, Warner RR (2006) Currents shifts and kin aggregation explain genetic patchiness in fish recruits. Ecology 87:3082–3094

    Article  Google Scholar 

  • Selkoe KA, Watson JR, White C, Ben Horin T, Iacchei M, Mitaral S, Siegel DA, Gaines SD, Toonen RJ (2010) Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species. Mol Ecol 19:3708–3726

    Article  Google Scholar 

  • Slatkin M (1977) Gene flow and genetic drift in a species subject to frequent local extinctions. Theor Pop Biol 12:253–262

    Article  CAS  Google Scholar 

  • Starr M, Himmelman JH, Therriault JC (1990) Direct coupling of marine invertebrate spawning with phytoplankton blooms. Science 247:1071–1074

    Article  CAS  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genome-wide experiments. Proc Natl Acad Sci USA 100:9440–9445

    Article  CAS  Google Scholar 

  • Thiébaut E, Cabioch L, Dauvin JC, Retière C, Gentil F (1997) Spatio-temporal persistence of the Abra alba-Pectinaria koreni muddy fine sand community of the eastern Bay of Seine. J Mar Biol Assoc UK 77:1165–1185

    Article  Google Scholar 

  • Van Oosterhout C, Hutchingson WF, Wills DPM, Shipley PF (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Wade MJ, McCauley DE (1988) Extinction and recolonization: their effects on the genetic differentiation of local populations. Evolution 42:995–1005

    Article  Google Scholar 

  • Waples RS (1989) A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121:379–391

    CAS  Google Scholar 

  • Waples RS (1990) TEMPTEST documentation, version 2.2. National Marine Fisheries Service, Seattle, WA

  • Waples RS, Do C (2008) L d N e: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Res 8:753–758

    Article  Google Scholar 

  • Weinmayr G, Vautrin D, Solignac M (1999) Isolation and characterization of highly polymorphic microsatellites from the Polychaete Pectinaria koreni. Mar Biotechnol 2:92–99

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • White C, Selkoe KA, Watson J, Siegel DA, Zacherl DC, Toonen RJ (2010) Ocean currents help explain population genetic structure. Proc R Soc Lond B 277:1685–1694

    Article  Google Scholar 

  • Wing SR, Gibbs MT, Lamare MD (2003) Reproductive sources and sinks within a sea urchin, Evechinus chloroticus, population of a New Zealand fjord. Mar Ecol Prog Ser 248:109–123

    Article  Google Scholar 

  • Wright S (1969) Evolution and the genetics of populations: the theory of gene frequencies, vol 2. University of Chicago Press, Chicago

    Google Scholar 

Download references

Acknowledgments

We are grateful to the crews of the RV “Côte d’Aquitaine” and RV “Côte de la Manche”. This work was co-financed by the “Programme National d’Environnement Côtier” and the “Institut Français pour la Biodiversité”, and MTJ acknowledges a grant from the Région Bretagne. Thanks to Nicolas Desroy for participation to cruises which enabled us to define areas of abundance for subsequent sampling in 2002, to the DEA 2003–2004 “Océanologie Biologique et Environnement Marin” for their help in measuring specimens and to the three anonymous referees for their constructive criticisms of the manuscript. Laboratory equipment was provided by the “Bettencourt-Schueller” Foundation and genotyping facilities by the “Plateforme Génopole Ouest” and “Génomer” based at the Station Biologique de Roscoff.

Author information

Authors and Affiliations

  1. Centre National de la Recherche Scientifique, UMR 7144, Laboratoire ‘Adaptation et Diversité en Milieu Marin’, Station Biologique de Roscoff, Place Georges Teissier, 29680, Roscoff, France

    M. T. Jolly, E. Thiébaut, F. Gentil & D. Jollivet

  2. Université Pierre et Marie Curie-Paris 6, Station Biologique de Roscoff, Roscoff, France

    M. T. Jolly, E. Thiébaut, F. Gentil & D. Jollivet

  3. School of Earth and Environmental Sciences, University of Portsmouth, Portsmouth, UK

    P. Guyard

Authors
  1. M. T. Jolly
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Thiébaut
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. Guyard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. Gentil
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D. Jollivet
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. Jollivet.

Additional information

Communicated by S. Uthicke.

Data accessibility: Original microsatellite data set is provided in DRYAD database, along with the corrected allele frequencies as an input file.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 37 kb)

Supplementary material 2 (TIFF 2932 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jolly, M.T., Thiébaut, E., Guyard, P. et al. Meso-scale hydrodynamic and reproductive asynchrony affects the source–sink metapopulation structure of the coastal polychaete Pectinaria koreni . Mar Biol 161, 367–382 (2014). https://doi.org/10.1007/s00227-013-2342-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-013-2342-1

Keywords

Search

Navigation