New paper on the influence of epigenetic effects on sex-specific fitness

Male Drosophila melanogaster.
Photo by André Karwath

Posted by Jessica Abbott.

Some colleagues and I published a paper in PLoS One a couple of months ago that I'd like to highlight here. We used male-limited X-chromosome evolution to investigate the influence of epigenetic effects on sex-specific fitness. The main aim of this experiment was actually to look for specialization of the X for male fitness as a result of the experimental evolution, but as a side effect we were able to look for imprinting effects. The experimental males received their sex chromsomes from the "wrong" parent (i.e. they had paternally inherited X's and maternally inherited Y's), which initially decreases male fitness, but which our experimental evolution lines were able to adapt to over time. We had thought that genomic imprinting was a possible explanation for this pattern, but an analysis of gene expression data suggested that the likely cause was rather maternal effects and coevolution between the sex chromosomes.

Epigenetics and Sex-Specific Fitness: An Experimental Test Using Male-Limited Evolution in Drosophila melanogaster. PLoS One 8(7): e70493.
By Jessica K. Abbott, Paolo Innocenti, Adam K. Chippindale, & Edward H. Morrow

Abstract: When males and females have different fitness optima for the same trait but share loci, intralocus sexual conflict is likely to occur. Epigenetic mechanisms such as genomic imprinting (in which expression is altered according to parent-of-origin) and sex-specific maternal effects have been suggested as ways by which this conflict can be resolved. However these ideas have not yet been empirically tested. We designed an experimental evolution protocol in Drosophila melanogaster that enabled us to look for epigenetic effects on the X-chromosome–a hotspot for sexually antagonistic loci. We used special compound-X females to enforce father-to-son transmission of the X-chromosome for many generations, and compared fitness and gene expression levels between Control males, males with a Control X-chromosome that had undergone one generation of father-son transmission, and males with an X-chromosome that had undergone many generations of father-son transmission. Fitness differences were dramatic, with experimentally-evolved males approximately 20% greater than controls, and with males inheriting a non-evolved X from their father about 20% lower than controls. These data are consistent with both strong intralocus sexual conflict and misimprinting of the X-chromosome under paternal inheritance. However, expression differences suggested that reduced fitness under paternal X inheritance was largely due to deleterious maternal effects. Our data confirm the sexually-antagonistic nature of Drosophila’s X-chromosome and suggest that the response to male-limited X-chromosome evolution entails compensatory evolution for maternal effects, and perhaps modification of other epigenetic effects via coevolution of the sex chromosomes.