Epigenetics and Sex-Specific Fitness: An Experimental Test Using Male-Limited Evolution in Drosophila melanogaster

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.

Paternal inheritance in mealybugs (Hemiptera: Coccoidea: Pseudococcidae)

“…This maternal effect was also attributed to environmental factors such as maternal diet (Wolf et al 1998). Paternal inheritance of the X chromosome in Drosophila melanogaster, which caused decreased male fitness, was also hypothesized to have maternal epigenetic effects (Abbot et al 2013). Moreover, the mealybug reproduction system is governed by an epigenetic process involving DNA imprinting by DNA methylation (Bongiorni et al 1999).…”

The microevolutionary response to male-limited X-chromosome evolution inDrosophila melanogasterreflects macroevolutionary patterns

“…In the control populations these females were wildtype LHM females, and in the MLX populations they were the backcrossed DX females. The total initial population size was therefore 960 individuals, but this was later reduced to 640 individuals (320 of each sex) for logistical reasons (Abbott et al 2013). The X-chromosome population size was inevitably lower in the MLX populations compared to the Control populations under this protocol, since females in the MLX populations do not carry wildtype X-chromosomes.…”

Sex‐linked inheritance, genetic correlations and sexual dimorphism in three melanin‐based colour traits in the barn owl

“…As a consequence, males who inherit the counter-selected femalelike version of a sexually antagonistically selected trait (and females who inherit a counter-selected malelike trait) may evolve compensatory strategies to reduce the cost of sexually antagonistic selection (e.g. Abbott et al, 2013).…”