Abstract
The past decades have witnessed extensive efforts to correlate fitness traits with genomic heterozygosity. While positive correlations are revealed in most of the organisms studied, results of no/negative correlations are not uncommon. There has been little effort to reveal the genetic causes of these negative correlations. The positive correlations are regarded either as evidence for functional overdominance in large, randomly mating populations at equilibrium, or the results of populations at disequilibrium under dominance. More often, the positive correlations are viewed as a phenomenon of heterosis, so that it cannot possibly occur under within-locus additive allelic effects. Here we give exact genetic conditions that give rise to positive and negative correlations in populations at Hardy-Weinberg and linkage equilibria, thus offering a genetic explanation for the observed negative correlations. Our results demonstrate that the above interpretations concerning the positive correlations are not complete or even necessary. Such a positive correlation can result under dominance and potentially under additivity, even in populations where associated overdominance due to linked alleles at different loci is not significant. Additionally, negative correlations and heterosis can co-occur in a single population. Although our emphasis is on equilibrium populations and for biallelic genetic systems, the basic conclusions are generalized to non-equilibrium populations and for multi-allelic situations.
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- Barker J. S. Inter-locus interactions: a review of experimental evidence. Theor Popul Biol. 1979 Dec;16(3):323–346. doi: 10.1016/0040-5809(79)90021-2. [DOI] [PubMed] [Google Scholar]
- Chakraborty R. The distribution of the number of heterozygous Loci in an individual in natural populations. Genetics. 1981 Jun;98(2):461–466. doi: 10.1093/genetics/98.2.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deng H. W., Lynch M. Change of genetic architecture in response to sex. Genetics. 1996 May;143(1):203–212. doi: 10.1093/genetics/143.1.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deng H. W., Lynch M. Estimation of deleterious-mutation parameters in natural populations. Genetics. 1996 Sep;144(1):349–360. doi: 10.1093/genetics/144.1.349. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fu Y. B., Ritland K. Marker-based inferences about epistasis for genes influencing inbreeding depression. Genetics. 1996 Sep;144(1):339–348. doi: 10.1093/genetics/144.1.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gaffney P. M., Scott T. M., Koehn R. K., Diehl W. J. Interrelationships of heterozygosity, growth rate and heterozygote deficiencies in the coot clam, Mulinia lateralis. Genetics. 1990 Mar;124(3):687–699. doi: 10.1093/genetics/124.3.687. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HALDANE J. B. S. The association of characters as a result of inbreeding and linkage. Ann Eugen. 1949 Oct;15(1):15–23. doi: 10.1111/j.1469-1809.1949.tb02418.x. [DOI] [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]
- KIMURA M., MARUYAMA T., CROW J. F. THE MUTATION LOAD IN SMALL POPULATIONS. Genetics. 1963 Oct;48:1303–1312. doi: 10.1093/genetics/48.10.1303. [DOI] [PMC free article] [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]
- Morton N. E., Crow J. F., Muller H. J. AN ESTIMATE OF THE MUTATIONAL DAMAGE IN MAN FROM DATA ON CONSANGUINEOUS MARRIAGES. Proc Natl Acad Sci U S A. 1956 Nov;42(11):855–863. doi: 10.1073/pnas.42.11.855. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ohta T. Slightly deleterious mutant substitutions in evolution. Nature. 1973 Nov 9;246(5428):96–98. doi: 10.1038/246096a0. [DOI] [PubMed] [Google Scholar]
- Pierce B. A., Mitton J. B. Allozyme heterozygosity and growth in the tiger salamander, Ambystoma tigrinum. J Hered. 1982 Jul-Aug;73(4):250–253. doi: 10.1093/oxfordjournals.jhered.a109633. [DOI] [PubMed] [Google Scholar]
- Schlager G., Dickie M. M. Natural mutation rates in the house mouse. Estimates for five specific loci and dominant mutations. Mutat Res. 1971 Jan;11(1):89–96. doi: 10.1016/0027-5107(71)90034-0. [DOI] [PubMed] [Google Scholar]
- Smit-McBride Z., Moya A., Ayala F. J. Linkage disequilibrium in natural and experimental populations of Drosophila melanogaster. Genetics. 1988 Dec;120(4):1043–1051. doi: 10.1093/genetics/120.4.1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Strauss S. H. Heterosis at Allozyme Loci under Inbreeding and Crossbreeding in PINUS ATTENUATA. Genetics. 1986 May;113(1):115–134. doi: 10.1093/genetics/113.1.115. [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]
- Zapata C., Alvarez G. On the detection of nonrandom associations between DNA polymorphisms in natural populations of Drosophila. Mol Biol Evol. 1993 Jul;10(4):823–841. doi: 10.1093/oxfordjournals.molbev.a040045. [DOI] [PubMed] [Google Scholar]
- Zouros E., Foltz D. W. The use of allelic isozyme variation for the study of heterosis. Isozymes Curr Top Biol Med Res. 1987;13:1–59. [PubMed] [Google Scholar]