Cytonuclear interactions and the economics of mating in seed beetles

Abstract

Recent studies have uncovered an abundance of nonneutral cytoplasmic genetic variation within species, which suggests that we should no longer consider the cytoplasm an idle intermediary of evolutionary change. Nonneutrality of cytoplasmic genomes is particularly intriguing, given that these genomes are maternally transmitted. This means that the fate of any given cytoplasmic genetic mutation is directly tied to its performance when expressed in females. For this reason, it has been hypothesized that cytoplasmic genes will coevolve via a sexually antagonistic arms race with the biparentally transmitted nuclear genes with which they interact. We assess this prediction, examining the intergenomic contributions to the costs and benefits of mating in Callosobruchus maculatus females subjected to a mating treatment with three classes (kept virgin, mated once, or forced to cohabit with a male). We find no evidence that the economics of mating are determined by interactions between cytoplasmic genes expressed in females and nuclear genes expressed in males and, therefore, no support for a sexually antagonistic intergenomic arms race. The cost of mating to females was, however, shaped by an interaction between the cytoplasmic and nuclear genes expressed within females. Thus, cytonuclear interactions are embroiled in the economics of mating.