A model for the evolution and control of generative apomixis

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A model is presented for the evolution and control of generative apomixis—a collective term for apomixis in animals and diplosporous apomixis in flowering plants. Its development takes into account data obtained from studies of apomictic-like processes in sexual organisms and in non-apomictic parthenogens, as well as data obtained from studies of generative apomicts. This approach provides insights into the evolution and control of generative apomixis that cannot be obtained from studies of generative apomicts alone. It is argued that the control of the avoidance of meiotic reduction during egg production in generative apomicts resides at a single locus, the identity of which can vary between lineages. This variation accounts for the observed variation between taxa in the pattern of avoidance of meiotic reduction. The affected locus contains a wild-type allele that codes for meiotic reduction and excess copies of a mutant allele that codes for its avoidance. The dominance relationship between these is determined by their ratio and by the environment. Environmental differences between female generative cells and somatic cells are such that the phenotypic expression of the mutant allele is favoured in the former, while that of the wild-type allele is favoured in the latter. This is important, for the locus is also involved in the control of mitosis which would be disrupted by the expression of the mutant allele in somatic cells. The requirement to maintain a viable pattern of growth and development explains why the wild-type allele is retained by generative apomicts, and this in turn explains why the ability to produce meiotically reduced eggs is retained by facultative forms and why it appears to be suppressed in, rather than absent from, obligate forms. The requirement for excess copies of the mutant allele in generative cells explains why generative apomicts are typically polyploid, as this condition provides a simple and effective means of generating the correct balance of mutant and wild-type alleles. Environmental effects can also lead to the dominance relationship between wild-type and mutant alleles varying between generative cells. In plants, this can lead to the apomixis gene being expressed, and thus to meiotic reduction being avoided, in only some ovules. Meiotically reduced, as well as meiotically unreduced, eggs are produced when this occurs. If compatible and viable pollen is available the meiotically reduced eggs may be fertilized, resulting in these organisms reproducing as facultative apomicts. It is argued that the control and evolution of parthenogenesis in generative apomicts varies between taxa. In some, the parthenogenetic initiation of embryos may result from the acquisition of a parthenogenesis gene or genes; but there is no reason to believe that this is either a general or a common requirement. Indeed, in some it may be an ancestral trait, these apomicts differing from their sexual ancestors in the ability to mature, rather than in the ability to initiate, embryos from unfertilized eggs; or it may result from physiological or developmental changes induced, for example, by polyploidization, hybridization, or the avoidance of meiotic reduction. In some plants it may be induced by pollination (without fertilization) or by the activity of a developing endosperm. Although it is argued that most generatively apomictic lineages may have acquired this form of reproduction relatively easily, by the acquisition of a mutation at a single locus, it is argued that newly initiated lineages may often be reproductively inefficient. These will begin to accumulate mutations that improve the efficiency of apomictic reproduction. Thus several loci may be involved in the control of generative apomixis in established lineages, even though only a single locus was involved in its initiation in these lineages. Care must be taken to distinguish between these initiator and modifier genes when considering the evolution of generative apomixis. Finally, it is argued that although generatively apomictic lineages have easily acquired this form of reproduction, its evolution in some taxa may be so difficult, requiring the acquisition of mutations simultaneously at two or more loci, that these may never acquire it. Thus, evidence obtained from taxa that have successfully made the transition from sexual reproduction to generative apomixis that its evolution was straightforward should not be used as evidence that its evolution will always be relatively easily achieved. Its uneven taxonomic distribution indicates that it is much more easily evolved by some taxonomic groups than by others.