Heteroplasmy and Organelle Gene Dynamics

This study assesses factors that influence the rates of change of organelle gene diversity and the maintenance of heteroplasmy. Losses of organelle gene diversity within individuals via vegetative segregation during ontogeny are paramount to resultant spatial and temporal patterns. Steady-state losses of organelle variation from the zygote to the gametes are determined by the effective number of organelles, which will be approximately equal to the number of intracellular organelles if random segregation prevails. Both rapid increases in organelle number after zygote formation and reductions at germ lines will reduce variation within individuals. Terminal reductions in organelles must be to very low copy numbers (<5) for substantial losses in variation to occur rapidly. Nonrandom clonal expansion and vegetative segregation during gametogenesis may be effective in reducing genetic variation in gametes. If organelles are uniparentally inherited, the asymptotic expectations for effective numbers of gametes and spatial differentiation will be identical for homoplasmic and heteroplasmic conditions. The rate of attainment of asymptote for heteroplasmic organelles, however, is governed by the rate of loss of variation during ontogeny. With sex-biased dispersal, the effective number of gametes is maximized when the proportional contributions of the sex having the higher dispersal rate are low.

AN APPROACH TO POPULATION AND EVOLUTIONARY GENETIC THEORY FOR GENES IN MITOCHONDRIA AND CHLOROPLASTS, AND SOME RESULTS

ABSTRACT We developed population genetic theory for organelle genes, using an infinite alleles model appropriate for molecular genetic data, and considering the effects of mutation and random drift on the frequencies of selectively neutral alleles. The effects of maternal inheritance and vegetative segregation of organelle genes are dealt with by defining new effective gene numbers, and substituting these for 2Ne in classical theory of nuclear genes for diploid organisms. We define three different effective gene numbers. The most general is N λ, defined as a function of population size, number of organelle genomes per cell, and proportions of genes contributed by male and female gametes to the zygote. In many organisms, vegetative segregation of organelle genomes and intracellular random drift of organelle gene frequencies combine to produce a predominance of homoplasmic cells within individuals in the population. Then, the effective number of organelle genes is Neo, a simple function of the numbers of males and females and of the maternal and paternal contributions to the zygote. Finally, when the paternal contribution is very small, Neo is closely approximated by the number of females, Nf. Then if the sex ratio is 1, the mean time to fixation or loss of new mutations is approximately two times longer for nuclear genes than for organelle genes, and gene diversity is approximately four times greater. The difference between nuclear and organelle genes disappears or is reversed in animals in which males have large harems. The differences between nuclear and organelle gene behavior caused by maternal inheritance and vegetative segregation are generally small and may be overshadowed by differences in mutation rates to neutral alleles. For monoecious organisms, the effective number of organelle genes is approximately equal to the total population size N. We also show that a population can be effectively subdivided for organelle genes at migration rates which result in panmixis for nuclear genes, especially if males migrate more than females.

Maintenance of genetic homogeneity in systems with multiple genomes

SUMMARYGenes or sequences of DNA present in multiple copies per cell include entire genomes of mitochondria and chloroplasts, nuclear ribosomal RNA genes, and highly repetitive sequences in heterochromatin. All copies are nearly identical, in spite of mutational pressure and weak selection. A zygote containing mitochondrial or chloroplast genophores of two different genotypes quickly produces progeny pure for one genotype or another (vegetative segregation). Evidence from yeast andChlamy-domonassuggests that organelle genophores undergo repeated rounds of random mating and recombination. When two molecules carrying different alleles at a locus recombine, gene conversion can result in the cell becoming pure for one allele. Stochastic matching and conversion (SMAC) has been studied by computer simulations which suggest that it will tend to eliminate new mutations in yeast mitochondrial DNA and speed up vegetative segregation. We have verified previous suggestions that gene conversion, occurring during unequal mitotic sister-strand crossing-over, provides an efficient mechanism for maintaining the homogeneity of repeated sequences in eukaryotic chromosomes.