Why are most organelle genomes transmitted maternally?

 http://onlinelibrary.wiley.com/doi/10.1002/bies.201400110/pdf

Mitochondrial DNA (mtDNA) is maternally inherited which means it does not undergo sexual recombination. But recombination is thought to be required to prevent an accumulation of mutations (a process known as Muller's ratchet, summarized below in red). Why do mitochondria survive then? How did maternal inheritance evolve?

Paternal leakage occurs

There is increasingly more evidence that occasionally sexual recombination does occur (known as paternal leakage) and this may slow down Muller's ratchet (this is only speculated). There is, however, a selection pressure towards the evolution of uniparental transmission.

Hypotheses for uniparental inheritance

Several theoretical models for the occurrence of uniparental organelle inheritance exist, including the following:

1. Avoiding competition between organelles and avoiding negative interaction between organelle genomes and/or other organelle genomes and the nuclear genome.
2. The genetic bottleneck makes it possible to get rid of mutations because genetic drift to homoplasmy can occur. Paternal leakage interferes with this process.
3. Many genes from endosymbionts have been transferred to the nuclear genome of the host cell and a lot of gene products are then re-imported into the endosymbiont. This means tight co-evolution and co-adaptation between endosymbiont and host cell is required. Mathematical models have shown that co-adaptation is enhanced by uniparental inheritance and could thus be the driving force of uniparental inheritance.

However, there are arguments against all of these hypotheses. For example, they fail to explain why , if uniparental transmission occurs, it is almost always maternal (uniparental paternal inheritance is very rare) and why killing of the paternal cytoplasm occurs (which can be costly).

In this paper, a unifying model for organelle inheritance is proposed.

They argue that uniparental inheritance evolved to avoid the spread of faster replicating organelle genomes that are incompatible with the host nucleus. This uniparental inheritance, however, is unstable (because of Muller's ratchet) and this drives a relaxation of strict maternal inheritance by paternal leakage or biparental transmission. Paternal leakage is then again susceptible to the evolution of fast replicating genomes incompatible with the host nucleus, so paternal leakage is lost again. Then it is restored again (because of Muller's ratchet), then lost again etc... They thus claim that uniparental inheritance is an unstable state. The maternal predominance is due to more mutations in the paternal cytotypes.

They then discuss some evidence for their theory.

Muller's ratchet

In asexual reproduction, genomes are inherited as indivisible blocks. If mutations occur, they will be carried over to the next generation. They will keep on accumulating and eventually the population will go extinct. In sexual reproduction, this is prevented because recombination occurs. Recombination allows for the possibility to generate genomes with fewer mutations from genomes that are highly mutated, by putting together mutation free portions of the parental chromosomes.

Note → Having a small genome reduces the probability of mutations to accumulate and therefore the effect of Muller's ratchet can be very small when genomes are small.