Can the associations between individual heterozygosity and viability, growth rate, and developmental stability arise as simple consequences of the control of flux in metabolic pathways by polymorphic enzymes? Haldane ( 1954) was the first to propose that heterozygotes at enzyme loci would be more efficient than homozygotes at controlling flux in metabolic pathways. This idea has been elaborated by others, each with different perspectives on the problem ( Berger 1976; Fincham 1972; Johnson 1974; Milkman 1967; Mitton and Koehn 1985; Clark and Koehn 1992). One way to envision superior control of metabolic flux is to assume that the genotypes have different biochemical properties under different conditions of temperature or pH and also that these environments fluctuate between conditions favoring first one homozygote and then another. This model was developed most extensively by Gillespie ( 1973, 1976, 1978a,b, 1991), and it is presented in a simple form in table 3.1, in which the various environmental conditions produce selective events in the life cycle. Note that the heterozygote has intermediate fitness in each of the environments but that it has the highest fitness when the genotypes experience both environments.
Empirical data regarding allozyme polymorphisms are often, but certainly not always, consistent with the theoretical expectation that components of fitness increase with heterozygosity. Studies comparing two portions of a life cycle often reveal viability differentials favoring heterozygous individuals. In populations, morphological variation and fluctuating asymmetry decrease with allozyme heterozygosity, indicating that developmental stability increases with heterozygosity. Growth rates and fecundity also increase with allozyme heterozygosity. All these relationships are easier to detect, or are more apparent, under a moderate degree of stress.
Physiological variation is associated with allozyme heterozygosity, and some of this variation is consistent with the advantages in viability, development, growth rate, and fecundity accruing to the highly heterozygous individuals. Routine metabolic costs, estimated from oxygen consumption in resting animals, decline with allozyme heterozygosity. The rate of protein cycling falls with allozyme heterozygosity, and this cost may explain the associations between resting oxygen consumption and heterozygosity.
Analyses of empirical data using the adaptive distance model suggest that some of the correlations between heterozygosity and components of fitness can be attributed to allozyme loci, or loci in strong linkage disequilibrium with them.