Uniparental inheritance of organelle genes

Because uniparental inheritance is so common, many biologists have supposed that it must have an evolutionary advantage over biparental inheritance. A number of hypothetical advantages have been proposed, but there are also potential disadvantages. The theories mirror those involved in the evolutionary advantages of sexual versus asexual reproduction, because uniparental inheritance reduces the opportunity for different individuals to exchange genes and produce recombinant genotypes — that is, for sexual reproduction. In the extreme case of strictly maternal (or paternal) inheritance, the mitochondrial or chloroplast genome is asexual, while the nuclear genome is sexual.One selective advantage of asexual reproduction is that it prevents the horizontal spread of selfish deleterious mutant genes and cytoplasmic parasites from one individual to another. Such elements can thus be transmitted only vertically, from parent to offspring, which limits their spread in the population. Similarly, uniparental inheritance prevents the horizontal transfer of selfish organelle genes. Such mutant genes are common in mitochondria, with examples including numerous types of respiratory deficient mutants such as poky in filamentous fungi, the petite mutants in yeast, and some mitochondrial mutants in humans. It is not known, however, whether selfish mutant genes are widespread in mitochondria of other organisms or in chloroplasts.A second advantage of uniparental inheritance (and of asexual reproduction in general) is that it prevents the breakup of advantageous organelle genotypes by outcrossing and recombination. This can provide an advantage when an organism occupies a stable environment but in general is probably overcome by the disadvantages of losing outcrossing and recombination.Perhaps the most important disadvantage of asexual reproduction is that natural selection is less effective in the absence of recombination and outcrossing. Thus uniparentally inherited organelle genomes, like asexual organisms, should tend to lose advantageous mutations and thus be less able to adapt to new ecological niches or changing environments. Additionally, uniparentally inherited genomes should tend to accumulate deleterious mutations faster than if they were inherited biparentally and recombined. This phenomenon, called Muller's ratchet, has been verified experimentally. If it is continued long enough, the cumulative effects of the deleterious mutations are expected to render the organelles and their critical genes nonfunctional.This raises the interesting questions: Why are we still alive? Why are there still any photosynthetic plants and algae? Here we will mention only two of the several possible answers. Muller's ratchet works because selection on linked genes in the genetic background interferes with selection at any site. But in the case of organelles, most of the genetic background consists of the nuclear genes, which are unlinked to the organelle genes and thus have little effect on selection. Consequently the ratchet may turn slowly enough to allow compensating mutations to cancel the effects of the deleterious mutations accumulating in the organelles. This is quite reasonable considering that most organelle gene products work in concert with numerous products of nuclear genes; for example in humans the mitochondrial ribosome consists of two mitochondrially encoded ribosomal RNAs joined with mitochondrial proteins encoded by nuclear genes. Any deleterious mutations in an organelle gene can probably be compensated by mutations at several sites in any of a number of interacting proteins.The theoretical advantages and disadvantages of uniparental inheritance are intriguing and one or another of these hypotheses is often uncritically accepted as the explanation for the prevalence of uniparental inheritance. But there is another alternative to these selective theories: uniparental inheritance may actually be effectively neutral, of little or no selective consequence for the organism. Then the frequency of uniparental inheritance would be determined principally by: the relative rates of transition from biparental to uniparental species and back, analogous to forward and backward mutation at the individual level; and the intensity of selection for other traits such as oogamy that may cause uniparental inheritance secondarily. None of these parameters is known for any organism.In fact, all of these factors must be considered in order to achieve a complete explanation for the relative frequencies of uniparental and biparental inheritance of organelle genes. Moreover, the explanation must be sought in a phylogenetic context in which the ancestral state of the organisms can be reconstructed. It may be more fruitful to analyze the evolution of mechanisms of uniparental inheritance (organelle exclusion from the zygote, selective silencing, and so on) as opposed to patterns. Given the complexity of the task, it will almost certainly be necessary to treat one limited group of organisms at a time, and combine them into successively larger trees to achieve more general explanations, or more likely, to show that the evolutionary consequences of uniparental inheritance vary from one group to another, just as the mechanisms vary.It should be clear from this Primer that uniparental inheritance is a quantitative trait with many different underlying mechanisms; moreover it is potentially subject to any or all of the evolutionary forces of mutation, random genetic drift, and selection within and between species. Unraveling the evolutionary history, causes, and consequences of the trait will almost certainly be much more difficult than we thought, and should provide many years of good scientific fun.