Skip to main content
Log in

Resource allocation and population genetics of the bay scallop, Argopecten irradians irradians: effects of age and allozyme heterozygosity on reproductive output

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The relationships among multiple-locus heterozygosity, age, reproduction and growth were examined over the ca. 2-yr lifespan of a cohort of northern bay scallops, Argopecten irradians irradians (Lamarck), from the Niantic River estuary, Connecticut, USA. Electrophoretic analyses revealed a relatively low proportion of polymorphic loci (=0.35) and low level of heterozygote deficiency ( D. across 6 loci=-0.05) in this population. Allele frequency distributions showed a high degree of temporal stability within and among cohorts. No significant correlation was found between multiple-locus heterozygosity and either somatic or reproductive growth. Our results lend support to the postulated linkage between low heterozygote deficit and lack of a heterozygosity/growth association in marine bivalves, and in the pectinid group in particular. Partial reproductive senility occurs in these scallops in their second year of life. Somatic tissue weight increased exponentially with increasing shell height, whereas pre-spawning gonad mass attained asymptotic values in 2-yr-old scallops. Thus, weight-specific reproductive effort was significantly lower in second- than first-year scallops (24 and 33% respectively). This pattern could be generated if high individual reproductive effort in the first year were correlated with accelerated (early) post-reproductive senescence. This kind of resource allocation, in which somatic growth is given precedence over reproductive growth in older individuals, has been previously reported in only one other bivalve, a pectinid (Chlamys islandica), in which the decline in reproductive effort occurs only after the scallops reach an age of ca. 20 yr.

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.

Institutional subscriptions

Similar content being viewed by others

Literature cited

  • Ahmad, M., Skibinski, D. O. F., Beardmore, J. A. (1977). An estimate of the amount of genetic variation in the common mussel Mytilus edulis. Biochem. Genet. 15: 833–846

    Google Scholar 

  • Barber, B. J., Blake, N. J. (1986). Reproductive effort and cost in the bay scallop, Argopecten irradians concentricus. Int. J. Invert. Reprod. Dev. 10: 51–57

    Google Scholar 

  • Bayne, B. L., Salkeld, P. N., Worrall, C. M. (1983). Reproductive effort and value in different populations of the marine mussel Mytilus edulis L. Oecologia 59: 18–26

    Google Scholar 

  • Beaumont, A. R. (1986). Genetic aspects of hatchery rearing of the scallop, Pecten maximus (L.). Aquaculture 57: 99–110

    Google Scholar 

  • Beaumont, A. R., Beveridge, C. M. (1984). An electrophoretic survey of genetic variation in Pecten maximus, Chlamys opercularis, C. varia and C. distorta from the Irish Sea. Mar. Biol. 81: 299–306

    Google Scholar 

  • Beaumont, A. R., Zouros, E. (1991). Genetics of scallops. In: Shumway, S. E. (ed.) Scallops: biology, ecology and aquaculture. Dev. in Aquaculture and Fisheries Science 21, Elsevier, New York, p. 585–623

    Google Scholar 

  • Beaumont, A. R., Gosling, E. M., Beveridge, C. M., Budd, M. D., Burnell, G. M. (1985). Studies on heterozygosity and size in the scallop, Pecten maximus. In: Gibbs, P. E. (ed.) Proc. 19th European Marine Biology Symposium. Cambridge University Press, Cambridge, p. 443–454

    Google Scholar 

  • Bricelj, V. M., Epp, J., Malouf, R. E. (1987a). Comparative physiology of young and old cohorts of bay scallops Argopecten irradians irradians (Lamarck): mortality, growth and oxygen consumption. J. exp. mar. Biol. Ecol. 110: 73–91

    Google Scholar 

  • Bricelj, V. M., Epp, J., Malouf, R. E. (1987b). Intraspecific variation in reproductive and somatic growth cycles of bay scallops Argopecten irradians. Mar. Ecol. Prog. Ser. 36: 123–137

    Google Scholar 

  • Calow, P. (1984). Exploring the adaptive landscapes of invertebrate life cycles. In: Engels, W., Clark W. H. Jr., Fischer, A., Olive, P. J. W., Went, D. F. (eds.) Advances in invertebrate reproduction 3, Proc. 3rd Int. Symp. Int. Soc. Invert. Reprod. Elsevier, New York, p. 329–342

    Google Scholar 

  • Charlesworth, B. (1980). Evolution in age-structured populations. In: Cannings, C., Hoppensteadt, F. (eds.) Cambridge studies in mathematical biology 1. Cambridge University Press, New York, p. 204–268

    Google Scholar 

  • Charlesworth, B., Leon, J. A. (1976). The relation of reproductive effort to age. Am. Nat. 110: 449–459

    Google Scholar 

  • Clarke, A. H. Jr. (1965). The scallop superspecies Aequipecten irradians (Lamarck). Malacologia 2: 161–188

    Google Scholar 

  • Comfort, A. (1979). The biology of senescence, 3rd edn. Churchill Livingstone, Edinburgh

    Google Scholar 

  • Dando, T. R., Storey, K. B., Hochachka, P. W. Storey, J. M. (1981). Multiple dehydrogenase in marine molluscs: electrophoretic analysis of alanopine dehydrogenase, strombine dehydrogenase, octopine dehydrogenase and lactate dehydrogenase. Mar. Biol. Lett. 2: 249–257

    Google Scholar 

  • Diehl, W. J., Koehn, R. K. (1985). Multiple-locus heterozygosity, mortality and growth in a cohort of Mytilus edulis. Mar. Biol. 88: 265–271

    Google Scholar 

  • Ernsting, G., Isaaks, J. A. (1991). Accelerated ageing: a cost of reproduction in the carabid beetle Notiophilus biguttatus. Funct. Ecol. 5: 299–303

    Google Scholar 

  • Fagen, R. M. (1972). An optimal life history in which reproductive effort decreases with age. Am. Nat. 104: 258–261

    Google Scholar 

  • Foltz, D. W., Zooros, E. (1984). Enzyme heterozygosity in the scallop Placopecten magellanicus (Gmelin) in relation to age and size. Mar. Biol. Lett. 5: 255–263

    Google Scholar 

  • Gadgil, M., Bossert, W. H. (1970). Life history consequences of natural selection. Am. Nat. 102: 52–64

    Google Scholar 

  • Gaffney, P. M., Scott, T. H., Koehn, R. K., Diehl, W. J. (1990). Interrelationships of heterozygosity, growth rate and heterozygote deficiencies in the coot clam, Mulinia lateralis. Genetics 124: 687–699

    Google Scholar 

  • Hawkins, A. J. S., Bayne, B. L., Day, A. J. (1986). Protein turnover, physiological energetics and heterozygosity in the blue mussel Mytilus edulis: the basis of variable age-specific growth. Proc. R. Soc. (Ser. B) 229: 161–176

    Google Scholar 

  • Hughes, R. N., Roberts, D. J. (1980). Reproductive effort of winkles (Littorina spp.) with contrasted methods of reproduction. Oecologia 47: 130–136

    Google Scholar 

  • Koehn, R. K., Shumway, S. E. (1982). A genetic/physiological explanation for differential growth rate among individuals of the oyster Crassostrea virginica (Gmelin). Mar. Biol. Lett. 3: 35–42

    Google Scholar 

  • Koehn, R. K., Milkman, R., Mitton, J. B. (1976). Population genetics of marine pelecypods. IV. Selection, migration and genetic differentiation in the blue mussel, Mytilus edulis. Evolution 30: 2–32

    Google Scholar 

  • Koehn, R. K., Diehl, W. J., Scott, T. M. (1988). The differential contribution by individual enzymes of glycolysis and protein catabolism to the relationship between heterozygosity and growth rate of the coot clam, Mulinia lateralis. Genetics 118: 121–130

    Google Scholar 

  • Koehn, R. K., Hall, J. G., Innes, D. J., Zera, A. J. (1984). Genetic differentiation of Mytilus edulis in eastern North America. Mar. Biol. 79: 117–126

    Google Scholar 

  • MacDonald, B. A. (1986). Production and resource partitioning in the giant scallop Placopecten magellanicus on the bottom and in suspended culture. Mar. Ecol. Prog. Ser. 34: 79–86

    Google Scholar 

  • Macleod, J. A. A., Thorpe, J. P., Duggan, N. A. (1985). A biochemical study of population structure in queen scallop (Chlamys opercularis) stocks in the Norther Irish Sea. Mar. Biol. 87: 77–82

    Google Scholar 

  • Marshall, N. (1960). Studies of the Niantic River, Connecticut, with special reference to the bay scallop, Aequipecten irradians. Limnol. Oceanogr. 5: 86–105

    Google Scholar 

  • Nichols, E. A., Ruddle, F. H. (1973). A review of enzyme polymorphism, linkage and electrophoretic conditions for mouse and somatic cell hybrids in starch gels. J. Histochem. Cytochem. 21: 1066–1081

    Google Scholar 

  • Perron, F. E. (1982). Inter- and intraspecific patterns of reproductive effort in four species of cone shells (Conus spp.). Mar. Biol. 68: 161–167

    Google Scholar 

  • Peterson, C. H. (1983). A concept of quantitative reproductive senility: application to the hard clam, Mercenaria mercenaria (L.). Oecologia 58: 164–168

    Google Scholar 

  • Pohle, D. G., Bricelj, V. M., Garcia-Esquivel, Z. (1991). The eelgrass canopy: an above-bottom refuge from benthic predators for juvenile bay scallops, Argopecten irradians. Mar. Ecol. Prog. Ser. 74: 47–59

    Google Scholar 

  • Rodhouse, P. G., McDonald, J. H., Newell, R. I. E., Koehn, R. K. (1986). Gamete production, somatic growth and multiple-locus enzyme heterozygosity in Mytilus edulis. Mar. Biol. 90: 209–214

    Google Scholar 

  • Scott, T. M., Koehn, R. K. (1990). The effect of environmental stress on the relationship of heterozygosity to growth rate in the coot clam Mulinia lateralis (Say). J. exp. mar. Biol. Ecol. 135: 109–116

    Google Scholar 

  • Selander, R. K. (1970). Behaviour and genetic variation in natural populations. Am. Zool. 10: 53–66

    Google Scholar 

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

    Google Scholar 

  • Singh, S. M. (1982). Enzyme heterozygosity associated with growth at different developmental stages in oysters. Can. J. Genet. Cytol. 24: 451–458

    Google Scholar 

  • Sokal, R. R., Rohlf, F. J. (1981). Biometry, 2nd edn. W. H. Freeman & Co., San Francisco

    Google Scholar 

  • Thompson, R. J., MacDonald, B. A. (1991). Physiological integrations and energy partitioning. In: Shumway, S. E. (ed.) Scallops: biology, ecology and aquaculture. Dev. in Aquaculture and Fisheries Science 21, Elsevier, New York, p. 347–376

    Google Scholar 

  • Vahl, O. (1984). Size-specific reproductive effort in (Chlamys islandica): reproductive senility or stabilizing selection? In: Gibbs, P. E. (ed.) Proc. 19th European Marine Biology Symposium. Cambridge Univ. Press, Cambridges, p. 521–527

    Google Scholar 

  • Volckaert, F., Zouros, E. (1989). Allozyme and physiological variation in the scallop Placopecten magellanicus and a general model for the effects of heterozygosity on fitness in marine molluscs. Mar. Biol. 103: 51–61

    Google Scholar 

  • Wall, J. R., Wall, S. W., Castagna, M. (1976). Enzyme polymorphisms and genetic variation in the bay scallop, Argopecten irradians. Genetics 83 (3, part 1) Suppl.: 81 (abstract)

    Google Scholar 

  • Williams, G. C. (1966). Adaptation and natural selection. Princeton University Press, New Jersey

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Zouros, E., Singh, S. M., Miles, H. (1980). Growth rate in oysters: an overdominant phenotype and its possible explanations. Evolution 34: 856–867

    Google Scholar 

  • Zouros, E., Singh, S. M., Foltz, D. W., Mallet, A. L. (1983). Post-settlement viability in the American oyster (Crassostrea virginica): an overdominant phenotype. Genet. Res. 41: 259–270

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by J. Grassle, New Brunswick

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bricelj, V.M., Krause, M.K. Resource allocation and population genetics of the bay scallop, Argopecten irradians irradians: effects of age and allozyme heterozygosity on reproductive output. Marine Biology 113, 253–261 (1992). https://doi.org/10.1007/BF00347279

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00347279

Keywords

Navigation