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Temporal stability of gene frequencies within genetically heterogeneous populations of the queen scallop Aequipecten (Chlamys) opercularis

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Abstract

The widely held assumption that gene frequencies within samples of multi-aged organisms are temporally stable has rarely been tested. In order to test this assumption in the commercially exploited bivalve scallop Aequipecten (Chlamys) opercularis (L.), 12 populations were sampled from around the UK over the period 1988–1990 and each was assayed at four putative polymorphic enzyme loci. Most populations were comprised of 3 to 4 year-classes, distinguishable by annual rings laid down on the shell. Three alleles from each locus were used as discriminant-function variables. Discriminant-function analysis based on allele frequencies averaged for each inividual year-class (45 demes) revealed highly significant inter-site heterogeneity. A posteriori classification of individual year-classes based on the discriminant analysis resulted in assignment of year-classes to the correct home site in 80% of cases. If allozyme neutrality is assumed, the phenomenon of predominant local allele frequency-stability through time within populations which are genetically heterogeneous from one site to another raises the possibility that queen scallop populations may be self-recruiting. Despite a planktonic larval phase lasting up to several weeks, this possibility is not excluded by the available hydrographic data.

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References

  • Aravindakshan I (1955) Studies on the biology of the queen scallop, Chlamys opercularis (L.) Unpublished thesis. University of Liverpool, Port Erin, Isle of Man

    Google Scholar 

  • Beacham TD, Withler RE, Murray CB, Barner LW (1988) Variation in body size, morphology, egg size, and biochemical genetics of pink salmon in British Columbia. Trans Am Fish Soc 117: 109–126

    Google Scholar 

  • Beaumont AR (1982) Geographic variation in allele frequencies at three loci in Chlamys opercularis from Norway to the Brittany coas. J mar biol Ass UK 62: 243–261

    Google Scholar 

  • Beaumont AR (1991) Allozyme data and scallop stock identification. J Cons int Explor Mer 47: 333–338

    Google Scholar 

  • Beaumont AR, Gosling EM, Beveridge CM, Budd MD, Burnell GM (1984) Studies on heterozygosity and size in the scallop, Pecten maximus Proc 19th Eur mar Biol Symp 443–454 [Gibbs PE (ed) University Press, Cambridge]

    Google Scholar 

  • Black KP, Moran PJ, Hammond LS (1991) Numerical models show coral reefs can be self-seeding. Mar Ecol Prog Ser 74: 1–11

    Google Scholar 

  • Bohlmeyer DA, Gold JR (1991) Genetic studies in marine fishes. II. A protein electrophoretic analysis of population structure in the red drum Sciaenops ocellatus. Mar Biol 108: 197–206

    Google Scholar 

  • Brand AR, Allison EH, Murphy EJ (1991a) North Irish sea scallop fisheries: a review of changes. In: Shumway SE, Sandifer PA (eds) World Aquaculture Workshops, Number 1 — An International Compendium of Scallop Biology and Culture. The World Aquaculture Society, Baton Rouge, Louisiana, pp 202–218

    Google Scholar 

  • Brand AR, Paul JD, Hoogesteger JN (1980) Spat settlement of the scallops Chlamys opercularis (L.) and Pecten maximus (L.) on artificial collectors. J mar biol Ass UK 60: 379–390

    Google Scholar 

  • Brand AR, Wilson UAW, Hawkins SJ, Allison EH Duggan NA (1991 b) Pectinid fisheries, spat collection, and the potential for stock enhancement in the Isle-of-Man. In: Lockwood SJ (ed) Ecology and management aspects of extensive mariculture. International Council for the Exploration of the sea, Copenhagen, pp 79–86 (ICES mar Sci Symp, Vol 192)

    Google Scholar 

  • Broom MJ (1976) Synopsis of biological data on scallops Chlamys (Aequipecten) opercularis (Linnaeus), Argopecten irradians (Lamarck), Argopecten gibbus (Linnaeus) FAO Fish Synopsis 114: 1–44

    Google Scholar 

  • Day AJ (1990) Microgeographic variation in allozyme frequencies in relation to the degree of exposure to wave action in the dogwhelk Nucella lapillus (L.) (Prosobranchia: Muricacae). Biol J Linn Soc 40: 245–261

    Google Scholar 

  • Dobzhansky T (1955) A review of some fundamental concepts and problems of population genetics. Cold Spring Harb Symp quant Biol 20: 1–15

    Google Scholar 

  • Ferguson A (1980) Biochemical systematics and evolution. Glasgow, Blackie

    Google Scholar 

  • Fevolden SE (1989) Genetic differentiation of the Icelandic scallop Chlamys islandica (Pectinidae) in the northern Atlantic Ocean. Mar Ecol Prog Ser 51: 77–85

    Google Scholar 

  • Freeman MF, Tukey JW (1950) Transformations related to the angular and the square root. Ann math Statist 21: 607–611

    Google Scholar 

  • Gilbert ES (1968) On discrimination using qualitative variables. J Am statist Ass 63: 1399–1412

    Google Scholar 

  • Harris H, Hopkinson DA (1978) Handbook of electrophoresis in human genetics. North-Holland, Amsterdam

    Google Scholar 

  • Heaps NS, Jones JE (1977) Density currents in the Irish Sea. Geophys J R astr Soc 51: 393–429

    Google Scholar 

  • Hoekstra RF, Bijlsma R, Dolman AJ (1985) Polymorphism from environmental heterogeneity: models are only robust if the heterozygote is close in fitness to the favored homozygote in each environment. Genet Res 45: 299–324

    Google Scholar 

  • Johnson GB (1976) Genetic polymorphism and enzyme function. In: Ayala FJ (ed) Molecular evolution. Sinauer, Sunderland, Mass, pp 46–59

    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

    Google Scholar 

  • Kacser H, Burns JA (1981) The molecular basis of dominance. Genetics, Austin, Tex 97: 639–666

    Google Scholar 

  • Kijima A, Mori K, Fujio Y (1984) Population differences in gene frequency of the japanese scallop Patinopecten yesoensis on the Okhotsk Sea coast of Hokkaido. Bull Jap Soc scient Fish 50: 241–248

    Google Scholar 

  • Koehn RK (1985) Adaptive aspects of biochemical and physiological variability. Proc 19th Eur mar Biol Symp 425–442 [Gibbs PE (ed) University Press, Cambridgel

    Google Scholar 

  • Koehn RK, Hilbish TJ (1987) The adaptive importance of genetic variation. Am Scient 75: 134–141

    Google Scholar 

  • Le Pennec M (1982) Delevage experimental de Chlamys opercularis (L.) (Bivalvia, Pectinidae). Vie mar 4: 29–36

    Google Scholar 

  • Lewis RI (1992) Population genetics of the queen scallop Clamys opercularis (L.) Unpublished thesis. University of Liverpool, Port Erin, Isle of Man

    Google Scholar 

  • Lewontin RC (1974) The genetic basis of evolutionary change. Columbia University Press, New York

    Google Scholar 

  • Macleod JAA, Thorpe JP, Duggan NA (1985) A biochemical study of population structure in queen scallop (Chlamys opercularis) stocks in the Northern Irish Sea. Mar Biol 87: 77–82

    Google Scholar 

  • Mason J (1957) The age and growth of the scallop, Pecten maximus (L.), in Manx waters. J mar biol Ass UK 36: 473–492

    Google Scholar 

  • Mathers NF (1975) Environmental variability at the phosphoglucose isomerase locus in the genus Chlamys. Biochem Syst Ecol 3: 123–127

    Google Scholar 

  • Moore DH (1973) Evaluation of five discrimination procedures for binary variables. J Am statist Ass 68: p 399

    Google Scholar 

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

    Google Scholar 

  • Nevo E, Beiles A, Ben-Schlomo R (1984) The evolutionary significance of genetic diversity: ecological, demographic and life history correlates. In: Mani GS, Levin S (eds) Lecture notes in biomathematics: evolutionary dynamics of genetic diversity. Springer-Verlag, Berlin, pp 13–212

    Google Scholar 

  • Nishida M, Lucas JS (1988) Genetic differences between geographic populations of the crown-of-thorns starfish throughout the Pacific region. Mar Biol 98: 359–368

    Google Scholar 

  • Norušis MJ (1992a) SPSS for windows base. ‘System users’ guide. Release 5. SPSS Inc, Michigan

    Google Scholar 

  • Norušis MJ (1992b) SPSS for windows. Professional statistics. Release 5. SPSS Inc, Michigan

    Google Scholar 

  • Paul JD (1978) The biology of the queen scallop, Chlamys opercularis (L.) in relation to its prospective cultivation. Unpublished thesis. University of Liverpool, Port Erin, Isle of Man

    Google Scholar 

  • Pickett GA, Franklin A (1975) The growth of queen scallops (Chlamys opercularis) in cages off Plymouth, south-west England. Int Counc Explor Sea (Comm Meet Pap Rep) K:25 1–4

  • Pingree RD, Griffiths DK (1978) Tidal fronts on the shelf seas around the British Isles. J geophys Res 83: 4615–4622

    Google Scholar 

  • Richardson BJ, Baverstock PR, Adams M (1986) Allozyme electrophoresis. Academic Press, Orlando

    Google Scholar 

  • Saavedra C, Zapata C, Guerra A, Alvare G (1993) Allozyme variation in European populations of the oyster Ostra edulis. Mar Biol 115: 85–95

    Google Scholar 

  • Sella G, Robotti CA, Biglione V (1993) Genetic divergence among three sympatric species of Mediterranean Patella (Archeogastropoda). Mar Biol 115: 401–405

    Google Scholar 

  • Shaw PR, Prasad R (1970) Starch gel electrophoresis of enzymes —a compilation of recipes. Biochem Genet 4: 297–320

    Google Scholar 

  • Sinclair M, Mohn RK, Probert G, Roddick DL (1985) Considerations for the effective management of Atlantic scallops. Can tech Rep Fish aquat Sciences 1382: 1–97

    Google Scholar 

  • Skibinski DOF, Beardmore JA, Cross TF (1983) Aspects of the population genetics of Mytilus (Mytilidae; Mollusca) in the British Isles. Biol J Linn Soc 19: 137–183

    Google Scholar 

  • Skibinski DOF, Woodwark M, Ward RD (1994) A quantitative test of the neutral theory using pooled allozyme data. Genetics (in press)

  • Smouse PE (1986) The fitness consequences of multiple-locus heterozygosity under the multiplicative overdominance and inbreeding depression models. Evolution 40: 946–957

    Google Scholar 

  • Soemodihardjo S (1974) Aspects of the biology of Chlamys opercularis (L.) (Bivalvia) with comparative notes on four allied species. Unpublished thesis. University of Liverpool, Port Erin, Isle of Man

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Bioemtry. The principles and practice of statistics in biological research. 2nd edn. WH Freeman & Co, New York

    Google Scholar 

  • Soule M (1976) Allozyme variation: its determinants in time and space. In: Ayala FJ (ed) Molecular evolution. Sinauer, Sunderland, Massachusetts, pp 60–77

    Google Scholar 

  • Taylor AC, Venn TJ (1978) Growth of the queen scallop Chlamys opercularis, from the Clyde Sea area. J mar biol Ass UK 58: 687–700

    Google Scholar 

  • Tracey ML, Bellet NF, Gravem CD (1975) Excess allozyme homozygosity and breeding population structure in the mussel Mytilus californianus. Mar Biol 32: 303–311

    Google Scholar 

  • Tremblay JM, Sinclair M (1990) Diel vertical migration of sea scallop larvae Placopecten magellanicus in a shallow embayment. Mar Ecol Prog Ser 67: 19–25

    Google Scholar 

  • Turelli M (1977) Random environments and stochastic calculus. Theor Popul Biol 12: 140–178

    Google Scholar 

  • Turelli M, Ginzberg L (1983) Should individual fitness increase with heterozygosity? Genetics, Austin, Tex 104: 191–209

    Google Scholar 

  • Valentine JW (1976) Genetic strategies of adaptation. In: Ayala FJ (ed) Molecular evolution. Sinauer, Sunderland, Massachusetts pp 78–94

    Google Scholar 

  • Ward RD, Beardmore JA (1977) Protein variation in the plaice (Pleuronectes platessa). Genet Res 30: 45–62

    Google Scholar 

  • Willis BL, Oliver JK (1990) Direct tracking of coral larvae: implications for dispersal studies of planktonic larvae in topographically complex environments. Ophelia 32: 145–162

    Google Scholar 

  • Wright S (1978) Evolution and the genetics of populations. Vol. 4. Variability within and among natural populations. Chapter 3: Genetic variability in natural populations: methods. University of Chicagio Press, Chicago, pp 79–103

    Google Scholar 

  • Zar JH (1984) Biostatistical analysis. 2nd edn. Prentice-Hall, Englewood Cliffs, New Jersey

    Google Scholar 

  • Zouros E (1987) On the relation between heterozygosity and heterosis: an evaluation of the evidence from marine molluscs. In: Rattazzi MC, Scandalios JG, Whitt GS (eds) Isozymes: current topics in biological and medical research. Vol 15. Alan R Liss, Inc, New York, pp 225–270

    Google Scholar 

  • Zouros E, Foltz DW (1984) Possible explanations for heterozygote deficiency in bivalve molluscs. Malacologia 25: 583–591

    Google Scholar 

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Communicated by J. Mauchline, Oban

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Lewis, R.I., Thorpe, J.P. Temporal stability of gene frequencies within genetically heterogeneous populations of the queen scallop Aequipecten (Chlamys) opercularis . Marine Biology 121, 117–126 (1994). https://doi.org/10.1007/BF00349480

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