Empirical testing of hypotheses about the evolution of genomic imprinting in mammals

Abstract

The close interaction between mother and offspring in mammals is thought to contribute to the evolution of genomic imprinting or parent-of-origin dependent gene expression. Empirical tests of theories about the evolution of imprinting have been scant for several reasons. Models make different assumptions about the traits affected by imprinted genes and the scenarios in which imprinting is predicted to have been selected for. Thus, competing hypotheses cannot readily be tested against each other. Further, it is far from clear how predictions about expression patterns of genes with specific phenotypic effects can be tested given current methodology of assaying gene expression levels, be it in the brain or in other tissues. We first set out a scenario for testing competing hypotheses and delineate the different assumptions and predictions of models. We then outline how predictions may be tested using mouse models such as intercrosses or recombinant inbred (RI) systems that can be phenotyped for traits relevant to imprinting theories. Further, we briefly discuss different molecular approaches that may be used in conjunction with experiments to ascertain expression patterns of imprinted genes and thus the testing of predictions.

Imprinting and its disorders in evolutionary perspective

“…Because resources must be carefully allocated between the mother, offspring, and siblings, it has been proposed that competition for resources imposes selective pressure on paternal and maternal genes. Therefore, maternally-derived genes favour resource-sparing for mother's future pregnancies while paternally-derived genes benefit from maximal resource exploitation during gestation, lactation, and later behavioural interactions among siblings (6,5,10). Indeed, some imprinted gene loci fit neatly into predictions of the kinship theory (for example, Igf2 is paternally expressed and has a positive effect on growth in juveniles, and H19 is maternally expressed and encodes an RNA that inhibits Igf2).…”

“…However, sexual antagonism creates a situation where the fittest alleles derive only from the same-sex parent and can cause a maladaptation in the opposite sex. Thus, imprinting is sometimes predicted to evolve when selection is much more stronger in one sex (5,10). In mammal populations females are typically the most demographically important sex; imprinting could elevate population fitness by allowing increasing and assymetric levels of adaptation only in females (5).…”

“…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.…”

“…Concerted evolution of both placentation and imprinting suggests that imprinting is involved in mother-offspring interactions (5,10). 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).…”

“…According to the kinship theory, multiple matings (multiple paternity) create unequal relatedness of fetuses and later individuals to their interactions with the mother and, on a bigger-scale, with individuals in a given population. All offspring of one mother have the same mother but different fathers (6,10). Because resources must be carefully allocated between the mother, offspring, and siblings, it has been proposed that competition for resources imposes selective pressure on paternal and maternal genes.…”