Dominance versus overdominance

Dominance versus overdominance is a controversy that has persisted for more than a century in genetics and plant breeding. Inbreeding depression is the loss of fitness that is observed, especially in small populations, due to loss of genetic diversity. Inbred strains tend to be homozygous for recessive alleles that are mildly harmful (or produce a trait that is undesirable from the standpoint of the breeder). Heterosis or hybrid vigor is the tendency of outbred strains to exceed both inbred parents in fitness.

Explaining hybrid vigor

When a population is small or inbred, it tends to lose genetic diversity. Selective breeding of plants and animals, including hybridization, began long before there was an understanding of underlying scientific principles. In the early 20th century, after Mendel's laws came to be understood and accepted, geneticists undertook to explain the superior vigor of many plant hybrids. Two competing hypotheses, which are not mutually exclusive, were developed:

• Dominance hypothesis. The dominance hypothesis attributes the superiority of hybrids to the suppression of undesirable recessive alleles from one parent by dominant alleles from the other. It attributes the poor performance of inbred strains to loss of genetic diversity, with the strains becoming purely homozygous at many loci.
• Overdominance hypothesis. Certain combinations of alleles that can be obtained by crossing two inbred strains are advantageous in the heterozygote. The overdominance hypothesis attributes to heterozygote advantage the survival of many alleles that are recessive and harmful in homozygotes. It attributes the poor performance of inbred strains to a high percentage of these harmful recessives.

Population geneticist James Crow, who in his younger days believed that overdominance was a major contributor to hybrid vigor, has undertaken a retrospective review of the developing science. According to Crow, the demonstration of several cases of heterozygote advantage in Drosophila and other organisms first caused great enthusiasm for the overdominance theory among scientists studying plant hybridization. But overdominance implies that yields on an inbred strain should decrease as inbred strains are selected for the performance of their hybrid crosses, as the proportion of harmful recessives in the inbred population rises. Over the years, experimentation in plant genetics has proven that the reverse occurs, that yields increase in both the inbred strains and the hybrids, suggesting that dominance alone may be adequate to explain the superior yield of hybrids. Only a few conclusive cases of overdominance have been reported in all of genetics. Since the 1980s, as experimental evidence has mounted, the dominance theory has made a comeback.

Crow writes, "The current view ... is that the dominance hypothesis is the major explanation of inbreeding decline and the high yield of hybrids. There is little statistical evidence for contributions from overdominance and epistasis. But whether the best hybrids are getting an extra boost from overdominance or favorable epistatic contributions remains an open question."

Genetic basis of heterosis

	Parental genotypes (homozygous)	Gene expression profile	Offspring genotype (heterozygous)	Gene expression profile
Scenario A	AA	1	Aa	1
	aa	0
Scenario B	AA	1	Aa	2
	aa	0 or 1
Dominance hypothesis . Scenario A . Less genes are under expressed in the homozygous individual. As well, gene expression in the offspring is equal to the expression of the best parent. Over dominance hypothesis . Scenario B . Over expression of certain genes in the homozygous. Legend 0 = low or no expression of gene A 1 = normal expression of gene A 2 = over expression of gene A]]

The two hypotheses (dominance and overdominance) have different consequences for the gene expression profile of the individuals. If over-dominance is the main cause for the fitness advantages of heterosis, then there should be an over-expression of certain genes in the heterozygous offspring compared to the homozygous parents. On the other hand, if dominance is the cause, then there should be fewer genes that are under-expressed in the heterozygous offspring compared to the parents. Furthermore, for any given gene, the expression should be comparable to the one observed in the best of the two parents.