Genomic Imprinting Leads to Less Selectively Maintained Polymorphism on X Chromosomes

Abstract

Population-genetic models are developed to investigate the consequences of viability selection at a diallelic X-linked locus subject to genomic imprinting. Under complete paternal-X inactivation, a stable polymorphism is possible under the same conditions as for paternal-autosome inactivation with differential selection on males and females. A necessary but not sufficient condition is that there is sexual conflict, with selection acting in opposite directions in males and females. In contrast, models of complete maternal-X inactivation never admit a stable polymorphism and alleles will either be fixed or lost from the population. Models of complete paternal-X inactivation are more complex than corresponding models of maternal-X inactivation, as inactivation of paternally derived X chromosomes in females screens these chromosomes from selection for a generation. We also demonstrate that polymorphism is possible for incomplete X inactivation, but that the parameter conditions are more restrictive than for complete paternal-X inactivation. Finally, we investigate the effects of recurrent mutation in our models and show that deleterious alleles in mutation-selection balance at imprinted X-linked loci are at frequencies rather similar to those with corresponding selection pressures and mutation rates at unimprinted loci. Overall, our results add to the reasons for expecting less selectively maintained allelic variation on X chromosomes.

Sex-Differential Selection and the Evolution of X Inactivation Strategies

“…When A 1 is sexually antagonistic ( i.e. , deleterious to females but beneficial to males), and with balancing selection acting at the A locus, the equilibrium frequencies of A 1 are:versions of which have been derived in several previous studies [43], [52]–[54]. The balancing selection criteria for sexually antagonistic polymorphism are provided (Text S1; for additional results and discussion, see [43], [52], [54]–[56]).…”

“…However, the parameter space that permits an X-linked sexually antagonistic polymorphism is larger under RXI than PXI, within the relevant parameter space where RXI can evolve (PXI can nevertheless be more conducive to polymorphism under alternative dominance parameterizations [52]), and recessive sexually antagonistic alleles that benefit males weakly can more readily be maintained [54], [71]. Therefore, the evolution of RXI could increase the parameter space that permits X-linked sexually antagonistic polymorphism.…”

Sexual antagonism and meiotic drive cause stable linkage disequilibrium and favour reduced recombination on the X chromosome

“…Several forms of natural selection – for example, antagonistic selection, fluctuating selection and heterozygote advantage – have been recognized for their purported roles in maintaining population genetic variation, and particular attention has been given to assessing which of these forms is most likely to account for variation found in nature (Prout, ). Additionally, several genetic properties, including dominance (Owen, ; Kidwell et al ., ; Fry, ), interaction with other genes (Patten et al ., ; Arnqvist et al ., ; Haig et al ., ) and transmission routes (Haldane, , ; Rice, , ; Hedrick & Parker, ; Patten & Haig, ,b; Jordan & Charlesworth, ; Santure & Spencer, ), have been examined for their influence on population genetic variation. Over time, a picture has emerged of how natural selection and the genetic system combine to shape patterns of polymorphism.…”