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Hierarchical population genetic structure in the commercially exploited shrimp Crangon crangon identified by AFLP analysis

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Abstract

The coastal shrimp Crangon crangon is an ecologically and commercially important species but there is limited knowledge of its genetic population structure. We utilised amplified fragment length polymorphisms (AFLPs) to investigate population differentiation among eight sampling locations comprising paired sites from north- and south-western Britain, the eastern English Channel and the Baltic Sea. Initial AMOVA and cluster analysis suggested strong differentiation, but outlier analysis identified three loci that might be subject to selection, one of which showed significant latitudinal variation in allele frequencies. Following exclusion of these outlier loci, and also of a divergent, genetically-impoverished sample from the UK Bristol Channel, cluster analysis revealed three major groupings, corresponding to geographical regions: western Britain, the eastern English Channel and the Baltic Sea. AMOVA identified significant differentiation both within and among these regions, with similar variation explained by each hierarchical level. C. crangon shows greater genetic structuring than has been found in many decapod crustaceans studied to date, and our results are consistent with unstable population sizes and gene flow restricted by distance and probably also hydrographic features. Further investigation of temporal stability in population structure is required, but broad-scale homogeneity of fishery stocks should not be assumed.

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References

  • Ball AO, Chapman RW (2003) Population genetic analysis of white shrimp, Litopenaeus setiferus, using microsatellite genetic markers. Mol Ecol 12:2319–2330

    Article  CAS  Google Scholar 

  • Barcia AR, Lopez GE, Hernandez D, Garcia-Machado E (2005) Temporal variation of the population structure and genetic diversity of Farfantepenaeus notialis assessed by allozyme loci. Mol Ecol 14:2933–2942

    Article  CAS  Google Scholar 

  • Bensch S, Åkesson M (2005) Ten years of AFLP in ecology and evolution: why so few animals? Mol Ecol 14:2899–2914

    Article  CAS  Google Scholar 

  • Benzie JAH (2000) Population genetic structure in penaeid prawns. Aquac Res 31:95–119

    Article  Google Scholar 

  • Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45

    Article  CAS  Google Scholar 

  • Bonnet E, Van de Peer Y (2002) ZT: a software tool for simple and partial Mantel tests. J Stat Soft 7:1–12

    Article  Google Scholar 

  • Borrell Y, Espinosa G, Romo J, Blanco G, Vázquez E, Sánchez JA (2004) DNA microsatellite variability and genetic differentiation among natural populations of the Cuban white shrimp Litoppenaeus schmitti. Mar Biol 144:327–333

    Article  CAS  Google Scholar 

  • Brooker AL, Benzie JAH, Blair D, Versini J-J (2000) Population structure of the giant tiger prawn Penaeus monodon in Australian waters, determined using microsatellite markers. Mar Biol 136:149–157

    Article  Google Scholar 

  • Bulnheim H-P, Schwenzer DE (1993) Population genetic studies on Crangon crangon and C. allmanni (Crustacea, Decapoda) from European coastal areas. Zool Jb Physiol 97:327–347 (in German)

  • Campbell D, Bernatchez L (2004) Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish genotypes. Mol Biol Evol 21:945–956

    Article  CAS  Google Scholar 

  • Corander J (2005) BAPS: Bayesian analysis of population structure manual vol 3.1 (updated 24/03/2005), http://www.rni.helsinki.fi/∼jic/bapspage.html

  • Corander J, Waldmann P, Sillanpää MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374

    CAS  PubMed  PubMed Central  Google Scholar 

  • Defra (2004) Department for the Environment, Fisheries and Rural Affairs, UK Sea Fisheries Statistics, http://www.statistics.Defra.gov.uk/esg/publications/fishstat/default.asp

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  Google Scholar 

  • Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) version 3.64. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

  • Fetzner JW Jr, Crandall KA (1999) Genetic variability within and among populations of the golden crayfish (Orconectes luteus): a comparison using amplified fragment length polymorphism (AFLPs) and mitochondrial 16S gene sequences. Freshw Crayfish 12:396–412

    Google Scholar 

  • Fratini S, Vannini M (2002) Genetic differentiation in the mud crab Scylla serrata (Decapoda: Portunidae) within the Indian Ocean. J Exp Mar Biol Ecol 272:103–116

    Article  CAS  Google Scholar 

  • Gomez-Uchida D, Weetman D, Hauser L, Galleguillos R, Retamal M (2003) Allozyme and AFLP analysis of genetic population structure in the hairy edible crab Cancer setosus from the Chilean coast. J Crustacean Biol 23:486–494

    Article  Google Scholar 

  • Gregory TR (2005) Animal genome size database, http://www.genomesize.com/. Last accessed 18/05/05

  • Harding GC, Kenchington EL, Bird CJ, Pezzack DS, Landry DC (1997) Genetic relationships among subpopulations of the American lobster (Homarus americanus) as revealed by random amplified polymorphic DNA. Can J Fish Aquat Sci 54:1762–1771

    Article  Google Scholar 

  • Hauser L, Adcock GJ, Smith PJ, Bernal-Ramirez JH, Carvalho GR (2002) Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proc Natl Acad Sci USA 99:11742–11747

    Article  CAS  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, Tracey M, Nelson K (1982) Genetics. In: Bliss DE (ed) The biology of Crustacea: embryology, morphology, and genetics. Academic, New York, pp 283–403

  • Henderson PA, Holmes RHA (1987) On the population biology of the common shrimp Crangon crangon (L.) (Crustacea: Caridea) in the Severn estuary and Bristol Channel. J Mar Biol Assoc UK 67:825–847

    Article  Google Scholar 

  • Henderson PA, Seaby R, Marsh SJ (1990) The population zoogeograpgy of the common shrimp Crangon crangon in British waters. J Mar Biol Assoc UK 70:89–97

    Article  Google Scholar 

  • Hoarau G, Boon E, Jongma DN, Ferber S, Palsson J, Van der Veer HW, Rijnsdorp AD, Stam WT, Olsen JL. (2005) Low effective population size and evidence for inbreeding in an overexploited flatfish, plaice (Pleuronectes platessa L.). Proc Biol Sci 272:497–503

    Article  Google Scholar 

  • Jolly MT, Jollivet D, Gentil F, Thiébault 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 

  • Kalinowski ST (2002) How many alleles per locus should be used to estimate genetic distances? Heredity 88:62–65

    Article  CAS  Google Scholar 

  • Lynch M, Milligan BG (1994) Analysis of population genetic structure with RAPD markers. Mol Ecol 3:91–99

    Article  CAS  Google Scholar 

  • Maggioni R, Rogers AD, Maclean N (2003) Population structure of Litoppenaeus schmitti (Decapoda: Penaeidae) from the Brazilian coast identified using six polymorphic microsatellite loci. Mol Ecol 12:3213–3217

    Article  CAS  Google Scholar 

  • McMillen-Jackson AL, Bert TM (2003) Disparate patterns of population structure and population history in two sympatric penaeid species (Farfantepenaeus aztecus and Litopenaeus setiferus) in the eastern United States. Mol Ecol 12:2895–2905

    Article  CAS  Google Scholar 

  • McMillen-Jackson AL, Bert TM (2004) Mitochondrial DNA variation and population genetic structure of the blue crab Callinectes sapidus in the eastern United States. Mar Biol 145:769–777

    CAS  Google Scholar 

  • Oh C-W, Hartnoll RG (2004) Reproductive biology of the common shrimp Crangon crangon (Decapoda: Crangonidae) in the central Irish Sea. Mar Biol 144:303–316

    Article  Google Scholar 

  • Oh C-W, Hartnoll RG, Nash RDM (1999) Population dynamics of the common shrimp, Crangon crangon (L.), in Port Erin Bay, Isle of Man, Irish Sea. ICES J Mar Sci 56:718–733

    Article  Google Scholar 

  • Ovenden JR, Street R, Peel D, Peel SL, Courtney AJ, Podlich HM, Basford KE, Dichmont CM (2004). A new data source for fisheries resource assessment: genetic estimates of the effective number of spawners. QO 04010 Queensland Government, Department of Primary Industries and Fisheries, p206, http://www.dpi.qld.gov.au/fishweb/16311.html

  • Page RDM (1996) Tree view: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2005) GenAlEx v.6: genetic analysis in excel. Population genetic software for teaching and research. Australian National University, Canberra, http://www.anu.edu.au/BoZo/GenAlEx/

  • Salomon JC, Breton M (1993) An atlas of long-term currents in the Channel. Oceanol Acta 16:439-448

    Google Scholar 

  • Siegel V, Gröger J, Neudecker T, Damm U, Jansen S (2005) Long-term variation in the abundance of the brown shrimp Crangon crangon (L.) population of the German Bight and possible causes for its interannual variability. Fish Oceanogr 14:1–16

    Article  Google Scholar 

  • Stamatis C, Triantafyllidis A, Moutou KA, Mamuris Z (2004) Mitochondrial DNA variation in northeast Atlantic and Meditteranean populations of Norway lobster Nephrops norvegicus. Mol Ecol 13:1377–1390

    Article  CAS  Google Scholar 

  • Takami Y, Koshio C, Ishii M, Fujii H, Hidaka T, Shimizu I (2004) Genetic diversity and structure of urban populations of Pieris butterflies assessed using amplified fragment length polymorphism. Mol Ecol 13:245–258

    Article  Google Scholar 

  • Temming A, Damm U (2002) Life cycle of Crangon crangon in the North Sea: a simulation of the timing of recruitment as a function of the seasonal temperature signal. Fish Oceanogr 11:45–58

    Article  Google Scholar 

  • Thorpe JP, Sole-Cava AM, Watts PC (2000) Exploited marine invertebrates: genetics and fisheries. Hydrobiologia 420:165–184

    Article  Google Scholar 

  • Triantafyllidis A, Apostolidis AP, Katsares V, Kelly E, Mercer J, Hughes M, Jørstad KE, Tsolou A, hynes R, Triantafyllidis C (2005) Mitochondrial DNA variation in the European lobster (Homarus gammarus) throughout its range. Mar Biol 146:223–235

    Article  CAS  Google Scholar 

  • Valles-Jimenez R, Cruz P, Perez-Enriquez R (2005) Population genetic structure of the Pacific white shrimp (Liopenaeus vannamei) from Mexico to Panama: microsatellite DNA variation. Mar Biotechnol 6:475–484

    Article  Google Scholar 

  • Vekemans X, Beauwens T, Lemaire M, Roldán-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol Ecol 11:139–151

    Article  CAS  Google Scholar 

  • Weber LI, Levy JA (2000) Genetic population structure of the swimming crab Callinectes danae (Crustacea: Decapoda) in southern Brazil. Hydrobiologia 420:203–210

    Article  Google Scholar 

  • Weber LI, Hartnoll RG, Thorpe JP (2000) Genetic divergence and larval dispersal in two spider crabs (Crustacea: Decapoda). Hydrobiologia 420:211–219

    Article  Google Scholar 

  • Weetman D, Hauser L, Carvalho GR (2001) Isolation and characterization of di- and trinucleotide microsatellites in the freshwater snail Potamopyrgus antipodarum. Mol Ecol Notes 1:185–187

    Article  CAS  Google Scholar 

  • Weetman D, Hauser L, Shaw PW, Bayes MK (2005) Microsatellite markers for the whelk Buccinum undatum. Mol Ecol Notes 5:361–362

    Article  CAS  Google Scholar 

  • Wilding CS, Butlin RK, Grahame J (2001) Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. J Evol Biol 14:611–619

    Article  CAS  Google Scholar 

  • Zhivotovsky L (1999) Estimating population structure in diploids with multilocus dominant DNA markers. Mol Ecol 8:907–913

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to members of the CEFAS Lowestoft Shellfish team, in particular Steven Lovewell and Peter Walker, and to Hans Francke and Cattriona Clemmsen for providing samples, and to the many others, who provided samples that could not be included in the present study. Jennifer Ovenden kindly provided a copy of an unpublished report on effective population size in Penaeus. We are also grateful to Craig Wilding for supplying a protocol upon which our AFLP methodology was based. We thank David Lunt and Africa Gomez for helpful discussion. This study conformed to UK and European legislation and guidance for the use of animals in scientific research and was funded by a grant to LH and PWS from the Department for Environment, Food and Rural Affairs (Defra project code MF0226).

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Authors and Affiliations

  1. Department of Biological Sciences, University of Hull, Hull, HU6 7RX, UK

    D. Weetman, A. Ruggiero, S. Mariani & L. Hauser

  2. Vector Group, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, L3 5QA, UK

    D. Weetman

  3. Department of Animal and Human Biology, University of La Sapienza, Rome, Italy

    A. Ruggiero

  4. Organon Ireland Limited, Drynam Road, Swords, County Dublin, Ireland

    A. Ruggiero

  5. School of Biological and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland

    S. Mariani

  6. School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK

    P. W. Shaw

  7. CEFAS Lowestoft Laboratory, Lowestoft, Suffolk, NR33 0HT, UK

    A. R. Lawler

  8. School of Aquatic and Fishery Sciences, University of Washington, 1122 NE Boat Street, 355020, Seattle, WA, 98195-5020, USA

    L. Hauser

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  1. D. Weetman
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  4. P. W. Shaw
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  5. A. R. Lawler
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  6. L. Hauser
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Correspondence to D. Weetman.

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Communicated by J. P. Thorpe, Port Erin.

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Weetman, D., Ruggiero, A., Mariani, S. et al. Hierarchical population genetic structure in the commercially exploited shrimp Crangon crangon identified by AFLP analysis. Mar Biol 151, 565–575 (2007). https://doi.org/10.1007/s00227-006-0497-8

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  • DOI: https://doi.org/10.1007/s00227-006-0497-8

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