Mitonuclear Ecology

Abstract

Eukaryotes were born of a chimeric union between two prokaryotes--the progenitors of the mitochondrial and nuclear genomes. Early in eukaryote evolution, most mitochondrial genes were lost or transferred to the nucleus, but a core set of genes that code exclusively for products associated with the electron transport system remained in the mitochondrion. The products of these mitochondrial genes work in intimate association with the products of nuclear genes to enable oxidative phosphorylation and core energy production. The need for coadaptation, the challenge of cotransmission, and the possibility of genomic conflict between mitochondrial and nuclear genes have profound consequences for the ecology and evolution of eukaryotic life. An emerging interdisciplinary field that I call "mitonuclear ecology" is reassessing core concepts in evolutionary ecology including sexual reproduction, two sexes, sexual selection, adaptation, and speciation in light of the interactions of mitochondrial and nuclear genomes.

Keywords: adaptation; coadaptation; genomic conflict; sexual reproduction; sexual selection; speciation.

Fig. 1.

Mitonuclear ecology is the study of how the interactions of mt and nuclear genomes shaped the nature of complex life. Mitonuclear interactions are proposed to have been the driving force behind the evolution of such quintessential eukaryotic characteristics as sexual reproduction involving two mating types, sexual selection and ornamentation, reproductively isolated species, and physiological adaptation. Arrows show potential consequences of evolutionary milestones.

Fig. 2.

A summary of key points of physical interaction of products of the mt genome (red) and the nuclear genome (blue), all of which occur on or within the inner mt membrane. Interactions of animal mt and N-mt genomes concern protein subunits of the electron transport system in complexes I, III, IV, and V (a) as well as interactions in the transcriptional (b) and translational (c, d) mechanisms needed to produce electron transport system proteins. There are two distinct mitonuclear interactions involved in translation.

Fig. 3.

The effects of sex linkage of N-mt genes on cotransmission, coevolution, genomic conflict, speciation, and ornamentation. Compatibility of nuclear and mt genes is color-coded: Blue is compatible with blue and orange with orange. The effects on F1 crosses are shown. The red star indicates offspring with total mt/N-mt incompatibility. Assuming that function is retained so long as one set of compatible genes is retained, then negative F1 effects occur only with Z linkage. For autosomal position and X linkage, incompatibility and function loss do not occur until the F2 hybrid generation.

Fig. 4.

The role of genetic changes to respiratory chain function in major adaptive radiations. In the transition from terrestrial locomotion to flight that accompanied the evolution of bats, there was strong selection for changes to the functional capacity of the respiratory chain to allow for increased ATP production to power flight muscles (Shen et al. 2010). In bats, 23% of the mt genes and about 5% of N-mt genes that code for OXPHOS proteins show evidence of positive selection, a proportion that is much higher than for non-OXPHOS N-mt genes or non-mt nuclear genes (left). Moreover, these rates of positive selection on OXPHOS genes are significantly higher in bats than in mice (left). Similarly in the evolution of snakes, nonsynonymous changes in mt OXPHOS genes, and particularly in cytochrome c oxidase subunit 1, suggest that a major shift in respiratory function accompanied the major shifts in body plan and prey consumption (Castoe et al. 2008) (right). The Alethinophidia lineage is the clade within all snakes with the greatest adaptive shifts. Deducing whether respiratory chain innovation leads or follows adaptive radiation will be a fascinating focus of future studies. Left panel redrawn from Shen et al. (2010) and right panel drawn from data in Castoe et al. (2008).