The evolution of genomic imprinting: theories, predictions and empirical tests

Abstract

The epigenetic phenomenon of genomic imprinting has motivated the development of numerous theories for its evolutionary origins and genomic distribution. In this review, we examine the three theories that have best withstood theoretical and empirical scrutiny. These are: Haig and colleagues' kinship theory; Day and Bonduriansky's sexual antagonism theory; and Wolf and Hager's maternal-offspring coadaptation theory. These theories have fundamentally different perspectives on the adaptive significance of imprinting. The kinship theory views imprinting as a mechanism to change gene dosage, with imprinting evolving because of the differential effect that gene dosage has on the fitness of matrilineal and patrilineal relatives. The sexual antagonism and maternal-offspring coadaptation theories view genomic imprinting as a mechanism to modify the resemblance of an individual to its two parents, with imprinting evolving to increase the probability of expressing the fitter of the two alleles at a locus. In an effort to stimulate further empirical work on the topic, we carefully detail the logic and assumptions of all three theories, clarify the specific predictions of each and suggest tests to discriminate between these alternative theories for why particular genes are imprinted.

Imprinting and its disorders in evolutionary perspective

“…If better fitness is expected with "matching" genotypes between the mother and the offspring, genetic covariance is favoured with silencing of paternal alleles. Conversely, if higher fitness interactions are achieved with "mismatching" genotypes, silencing of maternal alleles evolves (11). In viviparous species (where two genomes must coexist) with prolonged maternal care the offspring have higher fitness if they have a higher resemblance to their mother (6).…”

“…The kinship and coadaptation theories both derive fitness variation from social interactions. Not surprisingly, both theories predict imprinted expression in the organs of social interaction (for example, brain, endosperm, placenta) (11).…”

“…The maternal-offspringcoadaptation theory is based on a phenome non called epistasis (a phenomenon when interactions of certain genotypes result in a more (or less) than the sum of the interacting parts). Whenever interactions between traits affect fitness, genetic correlations are expected to evolve (11). If better fitness is expected with "matching" genotypes between the mother and the offspring, genetic covariance is favoured with silencing of paternal alleles.…”

“…The sexual antagonism theory relies on sex-specific selection pressures (10,11). In such a case, with time paternally-derived genes will become enriched for alleles of male benefit and maternally-derived ones for alleles of female benefit.…”

Genomic imprinting: theories and data

“…They argue that imprinting may have arisen for different reasons at different loci in different groups of organisms. In a similar vein, Patten et al (2014) compare and contrast three of the most prominent hypotheses, namely genetic conflict (Haig and Graham, 1991;Moore and Haig, 1991), sexual antagonism (Day and Bonduriansky, 2004) and maternal-offspring coadaptation (Wolf and Hager, 2006). They derive specific, discriminating predictions of these different ideas, which they hope will inspire empirical work aimed at testing these predictions.…”