Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-13T00:59:57.227Z Has data issue: false hasContentIssue false

The negative correlation between somatic aneuploidy and growth in the oyster Crassostrea gigas and implications for the effects of induced polyploidization

Published online by Cambridge University Press:  14 April 2009

E. Zouros*
Affiliation:
Department of Biology, The University of Crete, and Institute of Marine Biology of Crete, Iraklion, Crete, Greece Department of Biology, Dalhousie University, Halifax, N.S., CanadaB3H 4J1
C. Thiriot-Quievreux
Affiliation:
Observatoire Oceanologique, Université P. et M. Curie — CNRS, B.P. 28, F-06230, Villefranche-sur-Mer, France
G. Kotoulas
Affiliation:
Department of Biology, The University of Crete, and Institute of Marine Biology of Crete, Iraklion, Crete, Greece
*
* Corresponding author.
Rights & Permissions [Opens in a new window]

Summary

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

This study extends previous observations that chromosome loss in somaticcells of juveniles of the pacific oyster Crassostrea gigas is associated with reduced growth rate. All four studies designed to examine this association (two usingrandom population samples and two using full sibs) produced the same result. This consistent effect appears to be unrelated with the commonly, but not consistently, observed correlation between degree of allozyme heterozygosity and growth. We propose thatthe inverse relationship between aneuploidy and growth is due to the unmasking of deleterious recessive genes caused by ‘progressive haploidization’ of somatic cells. Because unmasking of deleterious recessive genes by random chromosome lossisunlikely in polyploid cells, this hypothesis may also provide an explanation for theobservation that artificially produced polyploid shellfish usually grow at faster rates than normal diploid ones.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

References

Audo, M. C., & Diehl, W. J., (1995). Effect of quantity and quality of environmental stress on multilocus heterozygosity-growth relationships in Eisenia fetida (Annelida: Oligochaeta). Heredity 75, 98105.CrossRefGoogle Scholar
Beaumont, A., & Fairbrother, J., (1991). Ploidy manipulation in molluscan shellfish: a review. Journal of Shellfish Research 10, 118.Google Scholar
Beaumont, A., Fairbrother, J., & Hoare, K., (1995). Multilocus heterozygosity and size: a test of hypotheses using triploid Mytilus edulis. Heredity 75, 256266.CrossRefGoogle Scholar
Beckenbach, A. T., (1994). Mitochondrial haplotype frequencies in oysters: neutral alternatives to selection models. In Non-neutral Evolution: Theories and Molecular Data (ed. B., Golding), pp. 188198. New York: Chapman and Hall.CrossRefGoogle Scholar
Borsa, P., Jusselin, Y., & Delay, B., (1992). Relationship between allozyme heterozygosity, body size, and survival to natural anoxic stress in the palourde Ruditapes decussatus L. (Bivalvia: Veneridae). Journal of Experimental Marine Biology and Ecology 155, 169181.CrossRefGoogle Scholar
Chang, B. H., Shimmin, L. C., Shyue, S. K., Hewett-Emmett, D., & Li, W.-H. (1994). Weak male-driven molecular evolution in rodents. Proceedings of the National Academy of Sciences of the USA 91, 827831.CrossRefGoogle ScholarPubMed
David, P., Delay, B., Berthou, P., & Jarne, P., (1995). Alternative models for allozyme-associated heterosis in the marine bivalve Spisula ovalis. Genetics 139,17191726.CrossRefGoogle ScholarPubMed
Foltz, D. W., (1986). Null alleles as a possible cause of heterozygote deficiencies in the oyster Crassostrea virginica and other bivalves. Evolution 40, 869870.CrossRefGoogle ScholarPubMed
Gaffney, P. M., Scott, T. M., Koehn, K., & Diehl, W. J., (1990). Interrelationships of heterozygosity, growth rate, and heterozygote deficiencies in the coot clam, Mulinia lateralis. Genetics 124, 687699.CrossRefGoogle ScholarPubMed
Gentilli, M. R., Beaumont, M. R., & Beaumont, A. R., (1988). Environmental stress, heterozygosity and growth rate in Mytilus edulis, L. Journal of Experimental Marine Biology and Ecology 129, 145153.CrossRefGoogle Scholar
Guo, X., Hershberger, W. K., Cooper, K., & Chew, K. K., (1992). Genetic consequences of blocking polar body I with Cytochalasin B in fertilized eggs of the Pacific oyster, Crassostrea gigas. II. Segregation of chromosomes. Biological Bulletin 183, 387393.CrossRefGoogle ScholarPubMed
Guo, X., & Allen, S. K., Jr (1994). Sex determination and polyploid gigantism in the dwarf surfclam Mulinia lateralis (Say). Genetics 138, 11991206.CrossRefGoogle ScholarPubMed
Hawkins, A. J. S., Day, A. J., Gérard, A., Naciri, Y., Ledu, C., Bayne, B. L., & Héral, M., (1994). A genetic and metabolic basis for faster growth among triploids induced by blocking meiosis I but not meiosis II in the larviparous European flat oyster, Ostrea edulis L. Journal of Experimental Marine Biology and Ecology 184, 2140.CrossRefGoogle Scholar
Hedgecock, D., & Sly, F., (1990). Genetic drift and effective population sizes of hatchery-propagated stocks of the Pacific oyster, Crassostrea gigas. Aquaculture 88, 2138.CrossRefGoogle Scholar
Houle, D., (1989). Allozyme-associated heterosis in Drosophila melanogaster. Genetics 123, 789801.CrossRefGoogle ScholarPubMed
Karl, S. A., & Avise, J. C., (1992). Balancing selection at allozyme loci in oysters: implications from nuclear RFLPs. Science 256, 100102.CrossRefGoogle ScholarPubMed
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 in the coot clam, Mulinia lateralis. Genetics 118, 121130.CrossRefGoogle Scholar
Longwell, A. C., & Stiles, S. S., (1968). Fertilization and completion of meiosis in spawned eggs of the American oyster Crassostrea virginica (Gmelin). Caryologia 21, 6573.CrossRefGoogle Scholar
Mukai, T., (1969). The genetic structure of natural populations of Drosophila melanogaster. VII. Synergistic interactions of mutant polygenes controlling viability. Genetics 61, 749761.CrossRefGoogle ScholarPubMed
Pasteur, N., Pasteur, G., Bonhomme, F., Catalan, J., & Britton-Davidian, J., (1988). Practical Isozyme Genetics. Chichester: Ellis Horwood.Google Scholar
Pogson, G. H., (1991). Expression of overdominance for specific activity at the phosphoglucomutase-2 locus in the Pacific oyster, Crassostrea gigas. Genetics 128, 133141.CrossRefGoogle ScholarPubMed
Pogson, G. H., & Zouros, E., (1994). Allozyme and RFLP heterozygosities as correlates of growth in the scallop Placopecten magellanicus: a test of the associative overdominance hypothesis. Genetics 137, 221231.CrossRefGoogle ScholarPubMed
Rodhouse, P. G., & Gaffney, P. M., (1984). Effect of heterozygosity on metabolism during starvation in the American oyster Crassostrea virginica. Marine Biology 80, 179187.CrossRefGoogle Scholar
Ruiz, A., & Barbadilla, A., (1995). The contribution of quantitative trait loci and neutral marker loci to the genetic variances and covariances among quantitative traits in random mating populations. Genetics 139, 445455.CrossRefGoogle Scholar
Scott, T. M., & Koehn, R. K., (1990). The effect of environmental stress on the relationship of heterozygosity to growth rate in coot clam Mulinia lateralis (Say). Journal of Experimental Marine Biology and Ecology 135, 109116.CrossRefGoogle Scholar
Shimmin, L. C., Chang, H.-J. & Li, W.-H. (1993). Maledriven evolution of DNA sequences. Nature 362, 745747.CrossRefGoogle ScholarPubMed
Stiles, S. S., & Longwell, A. C., (1973). Fertilization, meiosis and cleavage in eggs from large mass spawning of Crassostrea virginica (Gmelin), the commercial American oyster. Caryologia 26, 253262.CrossRefGoogle Scholar
Stiven, A. E., (1995). Genetic heterozygosity and growth rate in the southern appalachian land snail Mesodon normalis (Pilsbry 1900): the effects of laboratory stress. Malacologia 36, 171184.Google Scholar
Strathmann, T. S., (1987). Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast. University of Washington Press.Google Scholar
Thiriot-Quievreux, C., (1986). Etude de l'aneuploidie dans differents naissains d'Ostreidae (Bivalvia). Genetica (The Hague) 70, 225231.CrossRefGoogle Scholar
Thiriot-Quievreux, C., & Ayraud, N., (1982). Les caryotypes de quelques especers de Bivalves et Gasteropodes marins. Marine Biology 70, 165172.CrossRefGoogle Scholar
Thiriot-Quievreux, C, Noel, T., Bougrier, S., & Dallot, S., (1988). Relationships between aneuploidy and growth rate in pair matings of the oyster Crassostrea gigas. Aquaculture 75, 8996.CrossRefGoogle Scholar
Thiriot-Quievreux, C, Pogson, G. H., & Zouros, E., (1992). Genetics of growth rate variation in bivalves: aneuploidy and heterozygosity effects in a Crassostrea gigas family. Genome 35, 3945.CrossRefGoogle Scholar
Thomas, J. H., (1995). Genomic imprinting proposed as a surveillance mechanism for chromosome loss. Proceedings of the National Academy of Sciences of the USA 92, 480482.CrossRefGoogle ScholarPubMed
Zouros, E., (1987). On the relation between heterozygosity and heterosis: an evaluation of evidence from marine mollusks. Isozymes: Current Topics in Biological and Medical Research 15, 255279.Google ScholarPubMed
Zouros, E., Singh, S. M., & Miles, H. E., (1980). Growth rate in oysters: an overdominant phenotype and its possible explanations. Evolution 34, 856867.CrossRefGoogle ScholarPubMed
Zouros, E., & Foltz, D. W., (1987). The use of allelic isozyme variation for the study of heterosis. Isozymes: Current Topics in Biological and Medical Research 13, 159.Google Scholar