Abstract
Several studies have reported positive correlations between the degree of enzyme heterozygosity and fitness-related traits. Notable among these are the correlations between heterozygosity and growth rate in marine bivalves. Whether the correlation is the result of intrinsic functional differences between enzyme variants at the electrophoretic loci scored or arises from non-random genotypic associations between these loci and others segregating for deleterious recessive genes (the associative overdominance hypothesis) is a matter of continuing debate. A prediction of the associative overdominance hypothesis, not shared by explanations that treat the enzyme loci as causative agents of the correlation, is that the correlation is not specific to the type of genetic marker used. We have tested this prediction by scoring heterozygosity at single locus nuclear restriction fragment length polymorphisms (RFLPs) in a cohort of juvenile scallops (Placopecten magellanicus) in which growth rate was known to be positively correlated with an individual's degree of allozyme heterozygosity. A total of 222 individuals were scored for their genotypes at seven allozyme loci, two nonspecific protein loci of unknown function and eight nuclear RFLPs detected by anonymous cDNA probes. In contrast to the enzyme loci, no correlation was observed between growth rate and the degree of heterozygosity at the DNA markers. Furthermore, there was no relationship between the magnitude of heterozygote deficiency at a locus and its effect on the correlation. The differences observed between the effects of allozyme and RFLP heterozygosity on growth rate provide evidence against the associative overdominance hypothesis, but a strong case against this explanation must await corroboration from similar studies in different species.
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- Aquadro C. F., Desse S. F., Bland M. M., Langley C. H., Laurie-Ahlberg C. C. Molecular population genetics of the alcohol dehydrogenase gene region of Drosophila melanogaster. Genetics. 1986 Dec;114(4):1165–1190. doi: 10.1093/genetics/114.4.1165. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Budowle B., Giusti A. M., Waye J. S., Baechtel F. S., Fourney R. M., Adams D. E., Presley L. A., Deadman H. A., Monson K. L. Fixed-bin analysis for statistical evaluation of continuous distributions of allelic data from VNTR loci, for use in forensic comparisons. Am J Hum Genet. 1991 May;48(5):841–855. [PMC free article] [PubMed] [Google Scholar]
- Houle D. Allozyme-associated heterosis in Drosophila melanogaster. Genetics. 1989 Dec;123(4):789–801. doi: 10.1093/genetics/123.4.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jarman A. P., Wells R. A. Hypervariable minisatellites: recombinators or innocent bystanders? Trends Genet. 1989 Nov;5(11):367–371. doi: 10.1016/0168-9525(89)90171-6. [DOI] [PubMed] [Google Scholar]
- Jeffreys A. J., Royle N. J., Wilson V., Wong Z. Spontaneous mutation rates to new length alleles at tandem-repetitive hypervariable loci in human DNA. Nature. 1988 Mar 17;332(6161):278–281. doi: 10.1038/332278a0. [DOI] [PubMed] [Google Scholar]
- Koehn R. K., Diehl W. J., Scott T. M. 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. 1988 Jan;118(1):121–130. doi: 10.1093/genetics/118.1.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mallet A. L., Zouros E. A comment on the use of Nass's contingency test for random association of alleles at different loci. Heredity (Edinb) 1987 Aug;59(Pt 1):117–118. doi: 10.1038/hdy.1987.102. [DOI] [PubMed] [Google Scholar]
- Mitton J. B., Pierce B. A. The distribution of individual heterozygosity in natural populations. Genetics. 1980 Aug;95(4):1043–1054. doi: 10.1093/genetics/95.4.1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ota T. Associative overdominance caused by linked detrimental mutations. Genet Res. 1971 Dec;18(3):277–286. [PubMed] [Google Scholar]
- Pogson G. H. Expression of overdominance for specific activity at the phosphoglucomutase-2 locus in the Pacific oyster, Crassostrea gigas. Genetics. 1991 May;128(1):133–141. doi: 10.1093/genetics/128.1.133. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Riley M. A., Hallas M. E., Lewontin R. C. Distinguishing the forces controlling genetic variation at the Xdh locus in Drosophila pseudoobscura. Genetics. 1989 Oct;123(2):359–369. doi: 10.1093/genetics/123.2.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Riley M. A., Kaplan S. R., Veuille M. Nucleotide polymorphism at the xanthine dehydrogenase locus in Drosophila pseudoobscura. Mol Biol Evol. 1992 Jan;9(1):56–69. doi: 10.1093/oxfordjournals.molbev.a040708. [DOI] [PubMed] [Google Scholar]
- Singh R. S., Coulthart M. B. Genic variation in abundant soluble proteins of Drosophila melanogaster and Drosophila pseudoobscura. Genetics. 1982 Nov;102(3):437–453. doi: 10.1093/genetics/102.3.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tizard R., Cate R. L., Ramachandran K. L., Wysk M., Voyta J. C., Murphy O. J., Bronstein I. Imaging of DNA sequences with chemiluminescence. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4514–4518. doi: 10.1073/pnas.87.12.4514. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Turelli M., Ginzburg L. R. Should individual fitness increase with heterozygosity? Genetics. 1983 May;104(1):191–209. doi: 10.1093/genetics/104.1.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Voelker R. A., Schaffer H. E., Mukai T. Spontaneous Allozyme Mutations in DROSOPHILA MELANOGASTER: Rate of Occurrence and Nature of the Mutants. Genetics. 1980 Apr;94(4):961–968. doi: 10.1093/genetics/94.4.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zouros E. On the relation between heterozygosity and heterosis: an evaluation of the evidence from marine mollusks. Isozymes Curr Top Biol Med Res. 1987;15:255–270. [PubMed] [Google Scholar]
