A model for the evolution and control of generative apomixis

Abstract

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; ...

Non-Mendelian transmission of apomixis in maize–Tripsacum hybrids caused by a transmission ratio distortion

“…Moreover, whenever transmitted (c. 5 per cent of the BC 2 plants), apomixis is functionally expressed in simplex conditions in maize-Tripsacum dihaploid plants (Leblanc et al, 1996). Clearly, our results do not fit the allelic ratio hypotheses proposed by Mogie (1988) and Noirot (1993). The ratio of 'apomictic' vs. 'sexual' alleles in the dihaploids (10Mzǹ18Td; r = 0.5) and subsequent BC 3 plants (20Mzǹ18Td; r = 0.33) contradicts Mogie's model, in which apomixis arises when the ratio is more than 0.5.…”

“…It is conceivable, however, that different mechanisms might be acting with the same consequences. Hence, the models proposed by Mogie (1988) and Noirot (1993), even though they do not seem to apply in Tripsacum, might remain valid in other situations.…”

“…Therefore, apomixis would not be recovered in diploid plants. The second one proposes a dosage effect by which apomixis is not expressed in diploids, although the corresponding alleles may be transmitted (Mogie, 1988;Noirot, 1993). According to Mogie (1988), several copies of the gene(s) are required for normal apomictic development, and the 'sexual allele' is needed for the viable development of the embryo.…”

“…The second one proposes a dosage effect by which apomixis is not expressed in diploids, although the corresponding alleles may be transmitted (Mogie, 1988;Noirot, 1993). According to Mogie (1988), several copies of the gene(s) are required for normal apomictic development, and the 'sexual allele' is needed for the viable development of the embryo. In quite the reverse hypothesis, Noirot (1993) proposed that the 'apomictic allele' must be in a ratio of 0.25 or less to be functional.…”

Hybrid apomicts trapped in the ecological niches of their sexual ancestors

“…Significant differences are shown in bold. sexuals and polyploid apomicts in other agamic complexes is enhanced by reduced fertility in their hybrid progeny (48), reduced levels of backcrossing (e.g., in the R. auricomus complex) (63), and enhanced colonizing abilities for disturbed areas and species-range edges due to altered ecological tolerances (60,64), processes that would equally explain the more common pattern of ploidy-driven niche divergence within and across Boechera species. Our inability to identify geographic range size variation between reproductive modes (Table S3), or through divergence between geographic distance (i.e., latitude levels) and niche specificity (Table 1), underlines the importance of multiparametric analyses for tests of GP between reproductive groups.…”