The Effect of Genetic Conflict on Genomic Imprinting and Modification of Expression at a Sex-Linked Locus

Abstract

We examine how genomic imprinting may have evolved at an X-linked locus, using six diallelic models of selection in which one allele is imprintable and the other is not. Selection pressures are generated by genetic conflict between mothers and their offspring. The various models describe cases of maternal and paternal inactivation, in which females may be monogamous or bigamous. When inactivation is maternal, we examine the situations in which only female offspring exhibit imprinting as well as when both sexes do. We compare our results to those previously obtained for an autosomal locus and to four models in which a dominant modifier of biallelic expression is subjected to the same selection pressures. We find that, in accord with verbal predictions, maternal inactivation of growth enhancers and paternal inactivation of growth inhibitors are more likely than imprinting in the respective opposite directions, although these latter outcomes are possible for certain parameter combinations. The expected outcomes are easier to evolve than the same outcomes for autosomal loci, contradicting the available evidence concerning the direction of imprinting on mammalian sex chromosomes. In most of our models stable polymorphism of imprinting status is possible, a behavior not predicted by verbal accounts.

Population Models of Genomic Imprinting. II. Maternal and Fertility Selection

“…Previous models concerned with the evolution of imprinting from standard expression (Spencer et al 1998(Spencer et al , 2004 have found a similar result, but these latter models all involved both imprintable and unimprintable alleles. Pearce and Spencer (1992) investigated the effect of imprinting on standard models of viability selection.…”

Non-conflict theories for the evolution of genomic imprinting

“…Consequently, X-linked traits with different male and female optima should be selected to be imprinted to take advantage of this mechanism for differential male/female expression and, moreover, X-linked growth enhancers should be maternally active in most eutherians as males are general larger than females. This prediction, the opposite of that of the genetic conflict model (even as applied to X-chromosome inactivation; see Spencer et al, 2004), explains the monosomic mouse data (Iwasa and Pomiankowski, 1999).…”

Coadaptation and conflict, misconception and muddle, in the evolution of genomic imprinting

“…Benefits of 'resemblance' that have been proposed to explain the evolution of parent-specific expression include: paternally-inherited antigens of the placenta are silenced to avoid mismatch between maternal and fetal antigens (Elinson, 1989); maternally-derived genes are silenced to increase a child's resemblance to its father and thereby increase the amount of paternal care the child receives (Christenfeld and Hill, 1995); imprinting matches the size of a baby's head to the size of its mother's pelvis (Pembrey, 1996); inactivation of patrigenes in daughters and matrigenes in sons increases resemblance to samesex parents and enhances sex-specific fitness (Day and Bonduriansky, 2004); local adaptation is enhanced by matching offspring phenotype to the parent who disperses less (Spencer et al, 2004;Spencer and Clark, 2006). Wolf and Hager's (2006) model of 'maternal-offspring coadaptation' is often cited as the theoretical underpinning of the coadaptation hypothesis for the evolution of genomic imprinting.…”