Abstract
Many species of marine fish are typified by large population sizes, strong migratory behavior, high fecundity, and pelagic eggs and larvae that are passively transported by ocean currents, all features that tend to increase gene flow, and hence reduce genetic partitioning, among localized populations. The plaice, Pleuronectes platessa, is a commercially important demersal species that exhibits all of these characteristics. We analyzed genetic variation at eight microsatellite loci in samples of spawning adults (N = 348) from the coasts of Ireland, Iceland, and, for the first time, from the Baltic Sea. Significant differentiation was observed between Iceland and Irish and Baltic Sea samples. However, there were no genetic differences between Irish and Baltic Sea samples, which contrast with the significant differentiation reported between Baltic Sea and North Sea/Atlantic populations of other flatfish species. To increase the data set, we carried out a cross-calibration exercise, allowing us to perform a joint analysis of data with an earlier study on adult and juvenile plaice (N = 480) collected over a broad geographic range, using six microsatellite loci in common to the two studies. Significant differentiation was observed between fish collected at the northern (Iceland, Faeroes, Norway) and southern (Bay of Biscay) parts of the species range. In contrast, the results showed little evidence of genetic structuring over much of the continental shelf of Europe. We believe that bathymetric and hydrographic barriers are the major factors shaping genetic structure, while lack of structure over much of the European continental shelf may be explained by a combination of past historical events, population structure, and dynamics of the species.
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References
Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165
Begg GA (2005) Life history parameters. In: Cadrin SX, Friedland KD, Waldman JR (eds) Stock identification methods: applications in fishery science. Elsevier Academic Press, Oxford, pp 119–150
Belkhir K, Borsa P, Chikhi L et al (2000) GENETIX 4.01. Logiciel Sous Windows Pour la Génétique Des Populations. Laboratoire Génome et Populations. CNRS UPR 9060. Université de Montpellier II. Montpellier, France
Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188
Bouza C, Presa P, Castro J et al (2002) Allozyme and microsatellite diversity in natural and domestic populations of turbot (Scophthalmus maximus) in comparison with other Pleuronectiformes. Can J Fish Aquat Sci 59:1460–1473
Bradbury IR, Laurel BJ et al (2007) Defining ‘natal homing’ in marine fish populations: comment on Svedäng et al. (2007). Mar Ecol Prog Ser 349:307–308
Brookfield IFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5:453–455
Buonaccorsi VP, Westerman M, Stannard J et al (2004) Molecular genetic structure suggests limited larval dispersal in grass rockfish, Sebastes rastrelliger. Mar Biol 145:779–788
Cabranes C, Fernandez-Rueda P, Martínez JL (2008) Genetic structure of Octopus vulgaris around the Iberian Peninsula and Canary Islands as indicated by microsatellite DNA variation. ICES J Mar Sci 65:12–16
Cadrin SX, Friedland KD, Waldman JR (2005) Stock identification methods: applications in fishery science. Elsevier Academic Press, Oxford
Carlsson J, McDowell JR, Diaz-Jaimes P et al (2004) Microsatellite and mitochondrial DNA analyses of Atlantic bluefin tuna (Thunnus thynnus thynnus) population structure in the Mediterranean Sea. Mol Ecol 13:3345–3356
Chakraborty R, De Andrade M, Daiger SP, Budowle B (1992) Apparent heterozygote deficiencies observed in DNA typing data and their implications in forensic applications. Ann Hum Genet 56:45–57
Chapuris MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24(3):621–631
Charrier G, Durand J-D, Quiniou L, Laroche J (2006) An investigation of the population genetic structure of Pollack (Pollachius pollachius) based on microsatellite markers. ICES J Mar Sci 63:1705–1709
Charrier G, Coombs SH, McQuinn IH, Laroche J (2007) Genetic structure of whiting Merlangius merlangus in the Northeast Atlantic and adjacent waters. Mar Ecol Prog Ser 330:201–211
Cushing DH (1990) Plankton production and year class strength in fish populations: an update of the match/mismatch hypothesis. Adv Mar Biol 26:249–293
De Veen JF (1978) On selective tidal transport in the migration of North Sea plaice (Pleuronectes platessa) and other flatfish species. Neth J Sea Res 12:115–147
Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc B 39:1–38
Exadactylos A, Geffen AJ, Thorpe JP (1998) Population structure of the Dover sole, Solea solea L., in a background of high gene flow. J Sea Res 40:117–129
FAO (1965) Manual of sampling and statistical methods for fisheries biology. FAO Manuals in Fisheries Science. No. 1. Fasc. 9. Sec. 4:37–40
FAO (2007) The State of World Fisheries and Aquaculture 2006. FAO Fisheries and Aquaculture Department, Food and Agriculture Organisation of the United Nations, Rome 180
Florin A, Höglund J (2007) Absence of population structure of turbot (Psetta maxima) in the Baltic Sea. Mol Ecol 16:115–126
Florin A, Höglund J (2008) Population structure of flounder (Platichthys flesus) in the Baltic Sea: differences among demersal and pelagic spawners. Heredity 101:27–38
Fox CJ, MCLoCloghrie P, Young EF, Nash RDM (2006) The importance of individual behaviour for successful settlement of juvenile plaice (Pleuronectes platessa L.): a modelling and a field study in the eastern Irish Sea. Fish Oceanogr 15:301–313
Goudet J (2001) FSTAT. A program to estimate and test gene diversities and fixation indices 2.9.3. Institute of Ecology. University of Lausanne. Available at: http://www.unil.ch/izea/softwares/fstat.html
Guinand B, Lemaire C, Bonhomme F (2004) How to detect polymorphism undergoing selection in marine fishes? a review of methods and case studies, including flatfishes. J Sea Res 51:167–182
Guo SW, Thompson EA (1992) Performing the exact test for Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372
Hansen B, Østerhus S (2000) North Atlantic–Nordic Seas exchanges. Prog Oceanogr 45:109–208
Harden Jones FR (1968) Fish migration. Arnold, London
Hardie DC, Gillet RM, Hutchings JA (2006) The effects of isolation and colonisation history on the genetic structure of marine-relict populations of Atlantic cod (Gadus morhua) in the Canadian Arctic. Can J Fish Aquat Sci 63:1830–1839
Harding D, Nichols JH, Tungate DS (1978) The spawning of plaice (Pleuronectes platessa) in the southern North Sea and English Channel. Rapp P–V Réun CPIEM 172:102–113
Hemmer-Hansen J, Nielsen EEG, Grønkjær P, Loeschcke V (2007) Evolutionary mechanisms shaping the genetic population structure of marine fishes: lessons from the European flounder (Platichthys flesus L.). Mol Ecol 16:3104–3118
Hoarau G, Rijnsdorp AD, Van Der Veer HW et al (2002a) Population structure of plaice (Pleuronectes platessa L.) in northern Europe: microsatellites revealed large-scale spatial and temporal homogeneity. Mol Ecol 11:1165–1176
Hoarau G, Cook D, Stam WT, Olsen L (2002b) New microsatellite primers for plaice Pleuronectes platessa L. (Teleostei: Pleuronectidae). Mol Ecol 2:60–61
Hoarau G, Piquet AM-T, Van der Veer HW et al (2004) Population structure of plaice (Pleuronectes platessa L.) in northern Europe: a comparison of resolving power between microsatellites and mitochondrial DNA data. J Sea Res 51:183–190
Hoarau G, Boon E, Jongma DN et al (2005) Low effective population size and evidence for inbreeding in an overexploited flatfish, plaice (Pleuronectes platessa L.). Proc R Soc B 272:497–503
Hunter E, Metcalfe JD, Arnold GP (2003) Migration route and spawning fidelity in North Sea plaice. Proc R Soc Lond B 270:2097–2103
Hunter E, Metcalfe JD, Arnold GP, Reynolds JD (2004a) Impacts of migratory behaviour on population structure in North Sea plaice. J Anim Ecol 73:377–385
Hunter E, Metcalfe JD, Holford BH, Arnold GP (2004b) Geolocation of free-ranging fish on the European continental shelf as determined from environmental variables II. Reconstruction of plaice ground tracks. Mar Biol 144:787–798
Hutchinson WF, Carvahlo GR, Rogers SI (2001) Marked genetic structuring in localized spawning populations of cod Gadus morhua in the North Sea and adjoining waters, as revealed by microsatellites. Mar Ecol Prog Ser 223:251–260
ICES (1992) Report of the ICES Study Group on tagging experiments for juvenile plaice. ICES CM 1992/G:10, pp 40
ICES (2007) Report of the ICES Advisory committee on fishery management, advisory committee on the marine environment and advisory committee on ecosystems, 2007. ICES Advice Books 1–10
ICES (2008) Report of the ICES advisory committee on fishery management, advisory committee on the marine environment and advisory committee on ecosystems, 2008. ICES Advice Books 1–10
Johannesson K, André C (2006) Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Mol Ecol 15:2013–2029
Jørgensen HBH, Hansen MM, Bekkevold D et al (2005) Marine landscapes and population genetic structure of herring (Clupea harengus L) in the Baltic Sea. Mol Ecol 14:3219–3234
Jόnsdόttir ODB, Imsland AK, Daníelsdόttir AK, Marteinsdόttir G (2002) Genetic heterogeneity and growth properties of different genotypes of Atlantic cod (Gadus morhua L.) at two spawning sites off south Iceland. Fish Res 55:37–47
Karlsson S, Mork J (2005) Deviations from Hardy–Weinberg equilibrium, and temporal instability in allele frequencies at microsatellite loci in a local population of Atlantic cod. ICES J Mar Sci 62:1588–1596
Knutsen H, Jorde PE, Andre C, Stenseth C (2003) Fine-scaled geographical population structuring in a highly mobile marine species: the Atlantic cod. Mol Ecol 12:385–394
Lage C, Purcell M, Fogarty M, Kornfield I (2001) Microsatellite evaluation of haddock (Melanogrammus aeglefinus) stocks in the northwest Atlantic Ocean. Can J Fish Aquat Sci 58:982–990
Lind CE, Evans BS, Taylor JJU, Jerry DR (2007) Population genetics of a marine bivalve, Pinctada maxima, throughout the Indo-Australian Archipelago shows differentiation and decreased diversity at range limits. Mol Ecol 16:5193–5203
Lundy CJ, Rico C, Hewitt GM (2000) Temporal and spatial genetic variation in spawning grounds of European hake (Merlucius merlucius) in the Bay of Biscay. Mol Ecol 9:2067–2079
Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197
Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by ‘Monmonier’s algorithm’. Hum Biol 76:173–190
McQuinn IH (1997) Metapopulations and the Atlantic herring. Rev Fish Biol Fish 7:297–329
Metcalfe JD, Arnold GP (1997) Tracking fish with electronic tags. Nature 387:66–666
Metcalfe JD, Hunter E, Buckley AA (2006) The migratory behaviour of North Sea plaice: currents, clocks and clues. Mar Freshw BehavPhysiol 39:25–36
Millner R, Walsh SJ, Diaz de Astarloa JM (2005) Atlantic flatfish fisheries. In: Gibson RN (ed) Flatfishes: biology and exploitation. Blackwell Science, Oxford, pp 240–271
Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590
Nesbø CL, Rueness EK, Iversen SA et al (2000) Phylogeography and population history of Atlantic mackerel (Scomber scombrus L.): a genealogical approach reveals genetic structuring among eastern Atlantic stocks. Proc R Soc Lond B 267:281–292
Nielsen JG (1986) Pleuronectidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the north-eastern Alantic and the Mediterranean. UNESCO, UK, pp 1305–1306
Nielsen EE, Nielsen PH, Ruzzante DE et al (2004) Genetic population structure of turbot (Scophthalmus maximus L.) supports the presence of multiple hybrid zones for marine fishes in the transition zone between the Baltic Sea and the North Sea. Mol Ecol 13:585–595
Nielsen EE, Gronkjaer P, Meldrup D, Paulsen H (2005) Retention of juveniles within a hybrid zone between North Sea and Baltic Sea cod (Gadus morhua). Can J Fish Aquat Sci 62:2219–2225
O’Connell M, Wright JM (1997) Microsatellite DNA in fishes. Rev Fish Biol Fish 7:331–363
Paetkau D, Strobeck C (1995) The molecular basis and evolutionary history of a microsatellite null allele in bears. Mol Ecol 4:519–520
Pampoulie C, Ruzzante DE, Chosson V et al (2006) The genetic structure of Atlantic cod (Gadus morhua) around Iceland: insight from microsatellites, the Pan I locus, and tagging experiments. Can J Fish Aquat Sci 63:2660–2674
Pampoulie C, Stefánsson MO, Jörundsdóttir TG, Danilowicz BS, Daníelsdόttir AK (2008) Recolonization history and large-scale dispersal in the open sea: the case study of the North Atlantic cod Gadus morhua L. Biol J Linn Soc 9:315–329
Pingree RD (1993) Flow of surface waters to the west of the British Isles and in the Bay of Biscay. Deep-Sea Res (2 Top Stud Oceanogr) 40:369–388
Purdom CE, Wyatt T (1969) Racial differences in Irish Sea and North Sea plaice (Pleuronectes platessa). Nature 222:780–781
Purdom CE, Thompson D, Dando PR (1976) Genetic analysis of enzyme polymorphisms in plaice (Pleuronectes platessa). Heredity 37:193–206
Raymond M, Rousset F (1995) GENEPOP Version 1.2.: population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Reiss H, Hoarau G, Dickey-Collas M, Wolff WJ (2009) Genetic population structure of marine fish: mismatch between biological and fisheries management units. Fish Fish doi:10.1111/j.1467-2979.2008.00324.x
Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225
Rico C, Ibrahim KM, Rico I, Hewitt GM (1997) Stock composition in North Atlantic populations of whiting using microsatellite markers. J Fish Biol 51:462–475
Rijnsdorp AD (1989) Maturation of male and female North Sea plaice (Pleuronectes platessa L.). J Cons Int Explor Mer 46:35–51
Rijnsdorp AD (1991) Changes in fecundity of female North Sea plaice (Pleuronectes platessa L.) between three periods since 1900. ICES J Mar Sci 48:253–280
Rijnsdorp AD, Pastoors MA (1995) Modelling the spatial dynamics and fisheries of North Sea plaice (Pleuronectes platessa L.) based on tagging data. ICES J Mar Sci 52:963–980
Rijnsdorp AD, Millner RS (1996) Trends in population dynamics and exploitation of North Sea plaice (Pleuronectes platessa L.) since the late 1800 s. ICES J Mar Sci 53:1170–1184
Rijnsdorp AD, van Stralen M, der Veer HW (1985) Selective tidal transport of North Sea plaice larvae Pleuronectes platessa in coastal nursery areas. Trans Am Fish Soc 114:461–470
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228
Ruzzante DE, Taggart CT, Cook D (1996) Spatial and temporal variation in the genetic composition of a larval cod (Gadus morhua) aggregation: cohort contribution and genetic stability. Can J Fish Aquat Sci 53:2695–2705
Ruzzante DE, Wroblewski JS, Taggart CT et al (2000) Bay-scale population structure in coastal Atlantic cod in Labrador and Newfoundland, Canada. J Fish Biol 56:431–447
Ryan AW, Mattiangeli V, Mork J (2005) Genetic differentiation of blue whiting (Micromesistius poutassou Risso) populations at the extremes of the species range and at the Hebrides–Porcupine Bank spawning grounds. ICES J Mar Sci 62:948–955
Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York
Solmundsson J, Palsson J, Karlsson H (2005) Fidelity of mature Icelandic plaice (Pleuronectes platessa) to spawning and feeding grounds. ICES J Mar Sci 62:189–200
Spangler GR, Berst AH, Koonce JF (1981) Perspectives and policy recommendations on the relevance of the stock concept to fishery management. Can J Fish Aquat Sci 38:1908–1914
Steingrund P, Gaard E (2005) Relationship between phytoplankton production and cod production on the Faroe shelf. ICES J Mar Sci 62:163–176
Stepien CA (1999) Phylogeographical 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 8:923–939
Svedäng H, Righton D, Jonsson P (2007) Migratory behaviour of Atlantic cod Gadus morhua: natal homing is the prime stock-separating mechanism. Mar Ecol Prog Ser 345:1–12
Svendsen JIS, Alexanderson H, Astakhov V et al (2004) Late quaternary ice sheet history of northern Eurasia. Quatern Sci Rev 23:1229–1271
Thorrold SR, Latkoczy C, Swart PK, Jones CM (2001) Natal homing in a marine fish metapopulation. Science 291:297–299
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol 4:535–538
Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:438–450
Was A, Gosling EM, McCrann K, Mork J (2008) Evidence for population structuring of blue whiting (Micromesistius poutassou) in the Northeast Atlantic. ICES J Mar Sci 65:216–225
Watts PC, Nash RD, George SG, Kemp SJ (1999) Isolation and characterization of microsatellite loci in the European plaice Pleuronectes platessa L. (Teleostei: Pleuronectidae). Mol Ecol 8:2151–2152
Watts PC, Nash RD, George SG, Kemp SJ (2004) Genetic structure of juvenile plaice Pleuronectes platessa on nursery grounds within the Irish Sea. J Sea Res 51:191–197
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Acknowledgments
We thank Nóirín Burke, Gavin Power, Leszek Barcz, and Anna Danielsdóttir for providing samples, as well as the crew on the Marine Institute 2006 Irish Biological Survey and Polish Groundfish Surveys 2006 and 2007. Two anonymous reviewers provided very helpful comments on earlier versions of the paper. Funding was provided by the Department of Education, Ireland, under the Technological Sector Research Programme: Strand III Core Research Strengths Enhancement (2004–2007).
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Communicated by M. I. Taylor.
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Was, A., Gosling, E. & Hoarau, G. Microsatellite analysis of plaice (Pleuronectes platessa L.) in the NE Atlantic: weak genetic structuring in a milieu of high gene flow. Mar Biol 157, 447–462 (2010). https://doi.org/10.1007/s00227-009-1331-x
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DOI: https://doi.org/10.1007/s00227-009-1331-x