DELETERIOUS MUTATION ACCUMULATION IN ORGANELLE GENOMES

It is well established on theoretical grounds that the accumulation of mildly deleterious mutations in nonrecombining genomes is a major ext inction risk in obligately asexual populations. Sexual populations can also incur mutational deterioration in genomic regions that experienc e little or no recombination, i.e., autosomal regions near centromeres , Y chromosomes, and organelle genomes. Our results suggest, for a wid e array of genes (transfer RNAs, ribosomal RNAs, and proteins) in a di verse collection of species (animals, plants, and fungi), an almost un iversal increase in the fixation probabilities of mildly deleterious m utations arising in mitochondrial and chloroplast genomes relative to those arising in the recombining nuclear genome. This enhanced width o f the selective sieve in organelle genomes does not appear to be a con sequence of relaxed selection, but can be explained by the decline in the efficiency of selection that results from the reduction of effecti ve population size induced by uniparental inheritance. Because of the very low mutation rates of organelle genomes (on the order of 10(-4) p er genome per year), the reduction in fitness resulting from mutation accumulation in such genomes is a very long-term process, not likely t o imperil many species on time scales of less than a million years, bu t perhaps playing some role in phylogenetic lineage sorting on time sc ales of 10 to 100 million years.