Maternal transmission, sex ratio distortion, and mitochondria

Abstract

In virtually all multicellular eukaryotes, mitochondria are transmitted exclusively through one parent, usually the mother. In this short review, we discuss some of the major consequences of uniparental transmission of mitochondria, including deleterious effects in males and selection for increased transmission through females. Many of these consequences, particularly sex ratio distortion, have well-studied parallels in other maternally transmitted genetic elements, such as bacterial endosymbionts of arthropods. We also discuss the consequences of linkage between mitochondria and other maternally transmitted genetic elements, including the role of cytonuclear incompatibilities in maintaining polymorphism. Finally, as a case study, we discuss a recently discovered maternally transmitted sex ratio distortion in an insect that is associated with extraordinarily divergent mitochondria.symbiosis | cytoplasmic male sterility | Wolbachia | reproductive parasitism | genetic conflict B y virtue of their symbiotic origin, mitochondria are special (1). They have retained their own genome (with a few interesting exceptions), despite the fact that the vast majority of mitochondrial proteins are encoded in the much larger nuclear genome. A functioning organelle thus requires the tight regulation and coordination of two genomes with very different properties, histories, and locations. In addition, mitochondrial genomes reproduce asexually and are cytoplasmically inherited, typically through one sex, usually the female. This mode of transmission differs from most nuclear genomes, and has important consequences on an organism's fitness. There have been many excellent reviews on the different evolutionary trajectories of mitochondrial and nuclear genomes, including how these can result in genetic conflicts and incompatibility (e.g., refs. 2-10). In this short review we focus on the relationship between mitochondria and sex ratio distortion. We discuss how maternal transmission can drive the evolution of mitochondria (and other symbionts) that increase the frequency of females. We also consider how linkage between mitochondria and other maternally transmitted genetic elements, such as sex ratio distorters, can result in cytonuclear incompatibilities that may ultimately affect the persistence of the distorter. Finally, as a case study, we discuss a recently discovered maternally transmitted sex ratio distortion in a booklouse that is associated with extraordinarily divergent mitochondria.

Reliance of Wolbachia on High Rates of Host Proteolysis Revealed by a Genome-Wide RNAi Screen of Drosophila Cells

“…We suspect that the reduction of cellular ATP levels expected from knockdown of these genes limits the ability of Wolbachia to replicate within the cells. Alternatively, because specific Wolbachia and mitochondrial strains have coevolved, Wolbachia may be highly sensitive to functional changes in its companion mitochondria (Perlman et al 2015). It should be pointed out that some of these RNAi hits might be false positives because secondary screens have not confirmed them.…”

Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

“…Clark et al 2012;Phillips et al 2015). In addition, because most cytoplasmic genomes are inherited maternally, they can benefit from manipulating sexual reproduction to increase female reproduction and fitness (Perlman et al 2015). Examples of this phenomenon include chimeric ORFs in plant mitochondrial genomes that induce cytoplasmic male sterility (CMS; Ingvarsson and Taylor 2002;Touzet and Budar 2004;Fujii et al 2011) and numerous bacterial endosymbionts that manipulate sexual reproduction in animal hosts (Werren et al 2008).…”

Atypical mitochondrial inheritance patterns in eukaryotes

“…A strong association between mitochondria and sex determination has been observed in several eukaryotic taxa (e.g., Xu 2005;Chase 2007;Shakya and Idnurm 2014;Perlman et al 2015). For example, mitochondrial inheritance can be directly controlled by sex-determining genes, as in the fungus Phycomyces blakesleeanus (Shakya and Idnurm 2014).…”

“…Alternatively, mtDNA itself can be a key element in sex determination, as described below for several plant species with nuclear-cytoplasmic sex determining system (Bailey and Delph 2007;Chase 2007), or mtDNA can effect extreme sex ratio distortion, as recently demonstrated in the booklouse (specifically a strain referred to as Liposcelis nr. bostrychophila by Perlman et al (2015)). …”