ALBERT

Description: Mitochondrial interactions with the nuclear genome represent one of life’s most important co-evolved mutualisms. In many organisms, mitochondria are maternally inherited, and in these cases, co-transmission between the mitochondrial and nuclear genes differs across different parts of the nuclear genome, with genes on the X chromosome having two-third probability of co-transmission, compared with one-half for genes on autosomes. These asymmetrical inheritance patterns of mitochondria and different parts of the nuclear genome have the potential to put certain gene combinations in inter-genomic co-adaptation or conflict. Previous work in mammals found strong evidence that the X chromosome has a dearth of genes that interact with the mitochondria (mito-nuclear genes), suggesting that inter-genomic conflict might drive genes off the X onto the autosomes for their male-beneficial effects. Here, we developed this idea to test coadaptation and conflict between mito-nuclear gene combinations across phylogenetically independent sex chromosomes on a far broader scale. We found that, in addition to therian mammals, only Caenorhabditis elegans showed an under-representation of mito-nuclear genes on the sex chromosomes. The remaining species studied showed no overall bias in their distribution of mito-nuclear genes. We discuss possible factors other than inter-genomic conflict that might drive the genomic distribution of mito-nuclear genes.

Description: Two taxa studied to date, the therian mammals and Caenorhabditis elegans , display underrepresentations of mitonuclear genes (mt-N genes, nuclear genes whose products are imported to and act within the mitochondria) on their X chromosomes. This pattern has been interpreted as the result of sexual conflict driving mt-N genes off of the X chromosome. However, studies in several other species have failed to detect a convergent biased distribution of sex-linked mt-N genes, leading to questions over the generality of the role of sexual conflict in shaping the distribution of mt-N genes. Here we tested whether mt-N genes moved off of the therian X chromosome following sex chromosome formation, consistent with the role of sexual conflict, or whether the paucity of mt-N genes on the therian X is a chance result of an underrepresentation on the ancestral regions that formed the X chromosome. We used a synteny-based approach to identify the ancestral regions in the platypus and chicken genomes that later formed the therian X chromosome. We then quantified the movement of mt-N genes on and off of the X chromosome and the distribution of mt-N genes on the human X and ancestral X regions. We failed to find an excess of mt-N gene movement off of the X. The bias of mt-N genes on ancestral therian X chromosomes was also not significantly different from the biases on the human X. Together our results suggest that, rather than conflict driving mt-N genes off of the mammalian X, random biases on chromosomes that formed the X chromosome could explain the paucity of mt-N genes in the therian lineage.