Selfish Mitonuclear Conflict

Abstract

Mitochondria, a nearly ubiquitous feature of eukaryotes, are derived from an ancient symbiosis. Despite billions of years of cooperative coevolution - in what is arguably the most important mutualism in the history of life - the persistence of mitochondrial genomes also creates conditions for genetic conflict with the nucleus. Because mitochondrial genomes are present in numerous copies per cell, they are subject to both within- and among-organism levels of selection. Accordingly, 'selfish' genotypes that increase their own proliferation can rise to high frequencies even if they decrease organismal fitness. It has been argued that uniparental (often maternal) inheritance of cytoplasmic genomes evolved to curtail such selfish replication by minimizing within-individual variation and, hence, within-individual selection. However, uniparental inheritance creates conditions for cytonuclear conflict over sex determination and sex ratio, as well as conditions for sexual antagonism when mitochondrial variants increase transmission by enhancing maternal fitness but have the side-effect of being harmful to males (i.e., 'mother's curse'). Here, we review recent advances in understanding selfish replication and sexual antagonism in the evolution of mitochondrial genomes and the mechanisms that suppress selfish interactions, drawing parallels and contrasts with other organelles (plastids) and bacterial endosymbionts that arose more recently. Although cytonuclear conflict is widespread across eukaryotes, it can be cryptic due to nuclear suppression, highly variable, and lineage-specific, reflecting the diverse biology of eukaryotes and the varying architectures of their cytoplasmic genomes.

Fig. 1.. The balance of selection among different levels of organization.

Mitochondrial genomes that have a replication advantage can spread within an organism even if they confer deleterious effects on organismal function because selection on mitochondrial genomes acts both among and within individuals.

Fig 2.. Variation in mitochondrial inheritance.

(A) Representations of different modes of mitochondrial inheritance, including the doubly uniparental inheritance system in some bivalve molluscs [194, 195]. (B) Summary of studies of mitochondrial inheritance in major eukaryotic groups. (Left) Phylogenetic relationships of major eukaryotic clades as summarized by [1] and [196]. (Right) Grid of four columns (1-4, left to right) displaying information about our knowledge of mitochondrial inheritance in each group. (Col. 1) The number of studies pertaining to mitochondrial inheritance in each group. Few: 1-10 studies; Many: >> 10 studies. (Col. 2) The most common pattern of inheritance in each group based on current literature. Multiple colors per box indicate uncertainty about which pattern is most common. (Col. 3) Alternative patterns observed in the group. Strictly Uni.: Inheritance was found to be strictly uniparental and maternal; Bi. observed: Rare (<1% of individuals) cases of biparental inheritance were observed; Bi. common: biparental inheritance was observed in >1% of individuals. (Col. 4) A non-exhaustive list of references for mitochondrial inheritance in each group. (C) Non-maternal organelle inheritance in vascular plants. (Left) Phylogenetic relationships of major vascular plant clades as summarized by [197]. The double line for conifers represents possible non-monophyly [198]. (Right) Cases of mitochondria and plastid inheritance that depart from strictly maternal transmission including selected examples of genera in which these observations were made. Blank boxes indicate strict maternal inheritance. “No Data” indicates groups in which plastid/mitochondrial transmission in unknown. Modes of inheritance are abbreviated: P, paternal; PL, paternal leakage (similar to Bi. observed in panel B); B, biparental. References used to populate (C) include [27, 97, 117, 197-198, 217, 237-246].

Fig. 3.. Mechanisms of reproductive manipulation in cytoplasmic genomes.

Four mechanisms of reproductive parasitism of arthropods have been described in younger endosymbionts such as Wolbachia: Male killing/harm eliminates or reduces male functions, parthenogenesis results in asexual production of exclusively females, feminization causes males to develop as females, and cytoplasmic incompatibility prevents males with the selfish variant from mating with wildtype females. However, mitochondrial genomes have only been documented to cause male harm/killing, and evidence for plastids causing reproductive manipulation is scarce.