Selection on apomictic lineages of Taraxacum at establishment in a mixed sexual–apomictic population

A species’ mode of reproduction, sexual or asexual, will affect its ecology and evolution. In many species, asexuality is related to polyploidy. In Taraxacum, apomicts are triploid, and sexuals are diploid. To disentangle the effects of ploidy level and reproductive mode on life‐history traits, we compared established apomictic Taraxacum genotypes with newly synthesized apomictic genotypes, obtained from diploid–triploid crosses. Diploid–triploid crossing is probably the way that most apomictic lineages originate. New genotypes had on average a much lower seed set than established genotypes. Established genotypes differed on average from new genotypes, in particular under shaded conditions: the established genotypes had longer leaves and flowered later. The differences between new and established triploids resembled the differences that have been found between sexual diploids and established apomictic triploids. We conclude that ploidy differences alone are not directly responsible for observed differences between sexual diploid and apomictic triploid dandelions.     

Meiotic recombination in sexual diploid and apomictic triploid dandelions (Taraxacum officinale L.).

Taraxacum officinale L. (dandelion) is a vigorous weed in Europe with diploid sexual populations in the southern regions and partially overlapping populations of diploid sexuals and triploid or tetraploid apomicts in the central and northern regions. Previous studies have demonstrated unexpectedly high levels of genetic variation in the apomictic populations, suggesting the occurrence of genetic segregation in the apomicts and (or) hybridization between sexual and apomictic individuals. In this study we analysed meiosis in both sexual diploid and apomictic triploid plants to find mechanisms that could account for the high levels of genetic variation in the apomicts. Microscopic study of microsporocytes in the triploid apomicts revealed that the levels of chromosome pairing and chiasma formation at meiotic prophase I were lower than in that of the sexual diploids, but still sufficient to assume recombination between the homologues. Nomarski DIC (differential interference contrast) microscopy of optically cleared megasporocytes in the apomicts demonstrated incidental formation of tetrads, which suggests that hybridization can occur in triploid apomicts.     

A population dynamic model for facultative agamosperms

Plants that can reproduce both sexually and agamically are called facultative apomicts. Some species, such as Taraxacum, contain both sexual diploids and triploid facultative apomicts. Triploids produce seeds without gamete fusion and recombination, and can also produce pollen and fertilize diploids. We present a population dynamic model that deals with gene flow and competition between diploids and triploids, with differing allocation towards reproductive investment in seeds and pollen. This paper examines whether diploids and triploids of plants with facultative agamospermy can coexist within a single population. We analyse the global behavior of such a dynamic system. Features of the system are significantly affected by the germination rates of diploids and triploids. Either diploids or triploids persist alone when the germination rate of diploids is sufficiently larger or smaller than that of triploids, respectively. Competitive exclusion occurs when both germination rates are sufficiently large. Coexistence is possible under certain specific conditions when: (I) the germination rates of both diploid sexuals and triploids are not sufficiently large, and (II) triploids produce sufficient pollen. When diploid sexuals and triploids coexist, triploids cannot exist alone, implying that the pollen of triploids is necessary to exploit diploid ovules.     

Possible pathways of the gene flow inTaraxacum sect.Ruderalia

Reproductive behaviour and the pathways of gene flow among ploidy levels were studied experimentally inTaraxacum sect.Ruderalia. Diploid, triploid and tetraploid individuals were sampled from mixed diploid — polyploid natural populations. 136 experimental hybridizations between the plants of different ploidy levels were performed. Seeds resulting from these crosses, those obtained from isolated anthodia as well as from open pollinated anthodia (both from cultivated and wild plants) were subjected to the flow-cytometric seed screening (FCSS) to determine ploidy levels in the progeny and to infer breeding behaviour of maternal plants. Three possible pathways of the gene flow were studied: (A) fertilization of sexuals by pollen of apomicts, (B) B_III hybrid formation, (C) facultative apomixis. Diploid maternal plants when experimentally crossed with triploid pollen donors produced diploids and polyploid progeny, while when pollinated with a mixture of the pollen of diploids and triploids or insect pollinated, no polyploids were discovered. It seems that in the mixture with the pollen of diploids, the pollen of triploids is ineffective. Tetraploids produce hybrids much easier with diploid mothers and their role in wild populations requires further study. Triploid mothers, even those with subregular pollen did not show traces of facultative apomixis. B_III hybrids were present in the progeny of both triploids and tetraploids, in tetraploids in quite high percentages (up to 50% of the progeny in some crosses).     

Attack of the clones: reproductive interference between sexuals and asexuals in the Crepis agamic complex

Negative reproductive interactions are likely to be strongest between close relatives and may be important in limiting local coexistence. In plants, interspecific pollen flow is common between co‐occurring close relatives and may serve as the key mechanism of reproductive interference. Agamic complexes, systems in which some populations reproduce through asexual seeds (apomixis), while others reproduce sexually, provide an opportunity to examine effects of reproductive interference in limiting coexistence. Apomictic populations experience little or no reproductive interference, because apomictic ovules cannot receive pollen from nearby sexuals. Oppositely, apomicts produce some viable pollen and can exert reproductive interference on sexuals by siring hybrids. In the Crepis agamic complex, sexuals co‐occur less often with other members of the complex, but apomicts appear to freely co‐occur with one another. We identified a mixed population and conducted a crossing experiment between sexual diploid C. atribarba and apomictic polyploid C. barbigera using pollen from sexual diploids and apomictic polyploids. Seed set was high for all treatments, and as predicted, diploid–diploid crosses produced all diploid offspring. Diploid–polyploid crosses, however, produced mainly polyploidy offspring, suggesting that non‐diploid hybrids can be formed when the two taxa meet. Furthermore, a small proportion of seeds produced in open‐pollinated flowers was also polyploid, indicating that polyploid hybrids are produced under natural conditions. Our results provide evidence for asymmetric reproductive interference, with pollen from polyploid apomicts contributing to reduce the recruitment of sexual diploids in subsequent generations. Existing models suggest that these mixed sexual–asexual populations are likely to be transient, eventually leading to eradication of sexual individuals from the population.     

The Significance of Agamospermous Triploid Pollen Donors in the Sexual Relationships between Diploids and Triploids in Taraxacum (Compositae)

Abstract We review in this article the investigations of the significance of agamospermous triploid pollen donors in the sexual relationships between diploids and triploids in Taraxacum . Crossing experiments between diploid sexual mother plants and agamospermous polyploid pollen donors and recent isozyme analyses of the progeny have exhibited the following results: 1) Pollen from Agamospermous polyploid pollen donors have the potential to give rise to the polyploid agamospermous offspring when fertilizing diploid sexual plants. Ploidy level of the progeny is usually the same or higher, but occasionally lower, compared to the pollen donor. 2) Diploid progeny also occur from diploid (♀)-polyploid (♂) crosses, however, these diploids were in our results not hybrids but the results of self-fertilization of the diploids. The self-fertilization is regarded as a cosequence of the breakdown of the self-incompatibility barrier through the sterile triploid's pollen. This breakdown is in all probability a common phenomenon in diploid (♀)-polyploid (♂) crosses. Some examples suggest that agamospermous polyploids can increase their genetic diversity through obtaining genes from coexisting diploids. The evolutionary implications of this phenomenon and the reduction mechanism of chromosome number through agamospermous pollengenesis are discussed.     

Is polyploidy a persevering accident or an adaptive evolutionary pattern? The case of the brine shrimp Artemia

Asexual organisms are confronted with substantial drawbacks, both immediate and delayed, threatening their evolutionary persistence. Yet, genetic associations with asexuality may refresh the gene pool promoting adaptation of clonal lineages; polyploidy is one of them. Parthenogenesis itself and/or polyploidy are responsible for the maintenance and spread of clones in Artemia, a sexual-asexual genus of halophilic anostracans. We applied flow cytometry, microsatellite genotyping, and mtDNA sequencing to 23 asexual populations. Artemia parthenogens have evolved multiple times either through hybridization or spontaneously. Nine out of 23 populations contained clones of mixed ploidy (2n, 3n, 4n). Most clones were diploid (20/31) while two and nine clones were triploid and tetraploid, respectively. Apomictic triploids and tetraploids formed two distinct groups of low genetic diversity compared with the more divergent automictic diploids. Polyploidy is also polyphyletic in Artemia, with triploids and tetraploids having independent origins from different sexual ancestors. We discern a pattern of geographical parthenogenesis with all clonal groups being more widespread than their closest sexuals. In favour of a specialist model, asexual diploids are restricted to single locations and are strikingly segregated from generalist triploids and tetraploids occupying a variety of sites. This is a rare pattern of mixed life-history strategies within an asexual complex.     

Ecological and evolutionary opportunities of apomixis: insights from Taraxacum and Chondrilla

The ecological and evolutionary opportunities of apomixis in the short and the long term are considered, based on two closely related apomictic genera: Taraxacum (dandelion) and Chondrilla (skeleton weed). In both genera apomicts have a wider geographical distribution than sexuals, illustrating the short-term ecological success of apomixis. Allozymes and DNA markers indicate that apomictic populations are highly polyclonal. In Taraxacum, clonal diversity can be generated by rare hybridization between sexuals and apomicts, the latter acting as pollen donors. Less extensive clonal diversity is generated by mutations within clonal lineages. Clonal diversity may be maintained by frequency-dependent selection, caused by biological interactions (e.g. competitors and pathogens). Some clones are geographically widespread and probably represent phenotypically plastic 'general-purpose genotypes'. The long-term evolutionary success of apomictic clones may be limited by lack of adaptive potential and the accumulation of deleterious mutations. Although apomictic clones may be considered as 'evolutionary dead ends', the genes controlling apomixis can escape from degeneration and extinction via pollen in crosses between sexuals and apomicts. In this way, apomixis genes are transferred to a new genetic background, potentially adaptive and cleansed from linked deleterious mutations. Consequently, apomixis genes can be much older than the clones they are currently contained in. The close phylogenetic relationship between Taraxacum and Chondrilla and the similarity of their apomixis mechanisms suggest that apomixis in these two genera could be of common ancestry.     

On the origin and evolution of apomixis in Boechera

The genetic mechanisms causing seed development by gametophytic apomixis in plants are predominantly unknown. As apomixis is consistently associated with hybridity and polyploidy, these confounding factors may either (a) be the underlying mechanism for the expression of apomixis, or (b) obscure the genetic factors which cause apomixis. To distinguish between these hypotheses, we analyzed the population genetic patterns of diploid and triploid apomictic lineages and their sexual progenitors in the genus Boechera (Brassicaceae). We find that while triploid apomixis is associated with hybridization, the majority of diploid apomictic lineages are likely the product of intra-specific crosses. We then show that these diploid apomicts are more likely to sire triploid apomictic lineages than conspecific sexuals. Combined with flow cytometric seed screen phenotyping for male and female components of apomixis, our analyses demonstrate that hybridization is an indirect correlate of apomixis in Boechera.     

Inter-embryo competition in the progeny of autotriploid Aloineae (Liliaceae)

In reciprocal crosses between diploid and triploid Aloineae the progeny are largely diploid or diploid plus one or two chromosomes, but in reciprocal crosses between triploids and tetraploids they are tetraploid or nearly so. Thus the triploids contribute circa haploid gametes to the progeny when crossed with diploids but circa diploid gametes when crossed with tetraploids. These results are compared with those of a number of earlier workers. It is concluded that the bias in the frequency of progeny types towards diploidy or tetraploidy, depending on the ploidy level of the plant which is crossed with the triploid, is caused by inter-embryo competition. Those embryos with an endosperm/embryo factor of 1.5, the value found in normal diploid/diploid crosses having triploid endosperms, are selected in preference to those with factors higher or lower than 1.5.Inter-gamete competition also occurs among the euploid and aneuploid gametes produced by the triploids. This is more pronounced on the male side, because the degree of survival of aneuploid pollen from the triploids into the next generation is much lower than that of aneuploid egg nuclei.Non-reduction in the triploids gives rise to occasional pentaploid progeny in crosses with tetraploids, but it is more probable that in diploid/triploid crosses tetraploid progeny are the products of non-reduction in the diploid.     

Can obligate apomixis and more stable reproductive assurance explain the distributional successes of asexual triploids in Hieracium alpinum (Asteraceae)?

• Although reproductive assurance has been suggested to be one of the most important factors shaping the differential distributional patterns between sexuals and asexuals (geographic parthenogenesis), it has only rarely been studied in natural populations of vascular plants with autonomous apomixis. Moreover, there are almost no data concerning the putative relationship between the level of apomictic versus sexual plant reproduction on one hand, and reproductive assurance on the other.
• We assessed the level of sexual versus apomictic reproduction in diploid and triploid plants of Hieracium alpinum across its distributional range using flow cytometric analyses of seeds, and compared the level of potential and realized seed set, i.e. reproductive assurance, between the two cytotypes under field and greenhouse conditions.
• Flow cytometric screening of embryos and endosperms of more than 4,100 seeds showed that diploids produced solely diploid progeny sexually, while triploids produced triploid progeny by obligate apomixis. Potential fruit set was much the same in diploids and triploids from the field and the greenhouse experiment. While in the pollination‐limited environment in the greenhouse apomictic triploids had considerably higher realized fruit set than sexual diploids, there was no significant difference between cytotypes under natural conditions. In addition, sexuals varied to a significantly larger extent in realized fruit set than asexuals under both natural and greenhouse conditions.
• Our results indicate that triploid plants reproduce by obligate apomixis, assuring more stable and predictable fruit reproduction when compared to sexual diploids. This advantage could provide apomictic triploids with a superior colonisation ability, mirrored in a strong geographic parthenogenesis pattern observed in this species.

     

Fitness differences among diploids, tetraploids, and their triploid progeny in Chamerion angustifolium: mechanisms of inviability and implications for polyploid evolution

Abstract. Theoretical models indicate that the evolution of tetraploids in diploid populations will depend on both the relative fitness of the tetraploid and that of the diploid-tetraploid hybrids. Hybrids are believed to have lower fitness due to imbalances in either the ploidy (endosperm imbalance) or the ratio of maternal to paternal genomes in their endosperm (genomic imprinting). In this study we created diploids, tetraploids, and hybrid triploids of Chamerion angustifolium from crosses between field-collected diploid and tetraploid plants and evaluated them at six life stages in a greenhouse comparison. Diploid offspring (from 2 x × 2 x crosses) had significantly higher seed production and lower biomass than tetraploid offspring (from 4 x × 4 x crosses). Relative to the diploid, the cumulative fitness of tetraploids was 0.67. In general, triploids (from 2 x × 4 x , 4 x × 2 x crosses) had significantly lower seed production, lower pollen viability, and higher biomass than diploid individuals. Triploid offspring derived from diploid maternal parents had lower germination rates, but higher pollen production than those with tetraploid mothers. Relative to diploids, the cumulative fitness of 2 x × 4 x triploids and 4 x × 2 x triploids was 0.12 and 0.06, respectively, providing some support for effect of differing maternal:paternal ratios and endosperm development as a mechanism of hybrid inviability. Collectively, the data show that tetraploids exhibit an inherent fitness disadvantage, although the partial viability and fertility of triploids may help to reduce the barrier to tetraploid establishment in sympatric populations.     

The effect of intra-specific competition on seedlings of sexual and apomictic Taraxacum officinale

Because of their higher evolvability, sexuals may have an advantage relative to asexual organisms in a competitive environment with many biotic interactions. We tested this idea using sexual and apomictic Taraxacum , dandelions. Taraxacum seedlings were grown without competition and in different competing combinations in a greenhouse. Apomicts had more and longer leaves than sexuals, but the same dry weight at harvest as sexuals. Competition reduced growth to the same extent in both apomicts and sexuals. Therefore, we conclude that sexual dandelions are no superior competitors relative to apomicts. In Taraxacum , new apomictic lineages spin off from the sexual population with some unknown frequency. This may enable the apomictic community to keep up with the sexual population.     

GENETICAL POPULATION STRUCTURE IN PLANTS: GENE FLOW BETWEEN DIPLOID SEXUAL AND TRIPLOID ASEXUAL DANDELIONS (TARAXACUM SECTION RUDERALIA)

Levels and distribution of genetic variation were studied in central and western European populations of Taraxacum section Ruderalia containing differing mixtures of sexual diploid and asexual triploid plants. All sexual populations were panmictic with their variation partitioned mainly among populations. Genotypic diversity in triploid samples was very high with few clones widespread and many clones restricted to one or a few populations. Extensive amounts of gene (pollen) flow between the diploid and triploid components of a population were inferred from the following data: (1) the two ploidy levels share all major allozyme polymorphisms; (2) the intrapopulational homogeneity in genic variation between diploids and triploids contrasts strongly with the geographic differentiation at each ploidy level separately; (3) population-unique alleles simultaneously occur at the two ploidy levels; (4) not only sexuals but also asexuals generally simulate Hardy-Weinberg expectations. Most likely, intrapopulational gene exchange occurs bidirectionally by mechanisms such as reductional pollen meiosis in apomictic plants, facultative apomixis, and formation of unreduced gametes in sexuals. Thus, diploid and triploid Taraxacum section Ruderalia are less genetically isolated than has previously been supposed and probably form a cohesive evolutionary unit with the level at which gene pools are shared differing by population.     

Mating interactions between coexisting dipoloid, triploid and tetraploid cytotypes ofHieracium Echioides (Asteraceae)

Experimental crosses between diploids, triploids and tetraploids ofHieracium echioides were made to examine mating interactions. Specifically, cytotype diversity in progeny from experimental crosses, intercytotype pollen competition as a reproductive barrier between diploids and tetraploids, and differences in seed set between intra- and intercytotype crosses were studied. Only diploids were found in progeny from 2x × 2x crosses. The other types of crosses yielded more than one cytotype in progeny, but one cytotype predominated in each cross type: diploids (92%) in 2x × 3x crosses, tetraploids (88%) in 3x × 2x crosses, triploids (96%) in 2x × 4x crosses, triploids (90%) in 4x × 2x crosses, tetraploids (60%) in 3x × 3x crosses, pentaploids (56%) in 3x × 4x crosses, triploids (80%) in 4x × 3x crosses and tetraploids (88%) in 4x × 4x crosses. No aneuploids have been detected among karyologically analyzed plants. Unreduced egg cell production was detected in triploids and tetraploids, but formation of unreduced pollen was recorded only in two cases in triploids. Triploid plants produced x, 2x and 3x gametes: in male gametes x (92%) gametes predominated whereas in female gametes 3x (88%) gametes predominated. Cytotype diversity in progeny from crosses where diploids and tetraploids were pollinated by mixture of pollen from diploid and tetraploid plants suggested intercytotype pollen competition to serve as a prezygotic reproductive barrier. No statistically significant difference in seed set obtained from intra- and intercytotype crosses between diploids and tetraploids was observed, suggesting the absence of postzygotic reproductive barriers among cytotypes.     

Spatial ecological and genetic structure of a mixed population of sexual diploid and apomictic triploid dandelions

Ecological differentiation is widely seen as an important factor enabling the stable coexistence of closely related plants of different ploidy levels. We studied ecological and genetic differentiation between co-occurring sexual diploid and apomictic triploid Taraxacum section Ruderalia by analysing spatial patterns both in the distribution of cytotypes and in the distribution of genetic variation within and between the cytotypes. A significant relationship between ploidy level and elevation was found. This mode of ecological differentiation however, was not sufficient to explain the significant spatial structure in the distribution of diploids and triploids within the population. Strong congruence was found between the spatial genetic patterns within the diploids and within the triploids. We argue that this congruence is an indication of gene flow between neighbouring plants of different ploidy levels.     

二倍体鲫鲤F2产生不同倍性卵子的证据

在检测到鲫鲤F2产生3种不同大小(直径分别为0.13 cm,0.17cm和0.2 cm)类型的卵子基础上,进行了F2(♀)×红鲫(♂)及F2(♀)×四倍体鲫鲤(♂)的交配实验.通过染色体计数和流式细胞仪分析,在F2(♀)×红鲫(♂)后代中获得了四倍体、三倍体、二倍体鱼;在F2(♀)×四倍体鲫鲤(♂)后代中获得了四倍体和三倍体鱼.这两个交配组合后代中出现的不同倍性的鱼类为证明鲫鲤F2能产生三倍体、二倍体和单倍体卵子提供了进一步证据.F2(♀)×红鲫(♂)中雄性四倍体鱼的存在说明在四倍体后代中存在基因型为XXXY的个体.对上述两个交配组合后代的四倍体鱼和三倍体鱼的性腺结构观察表明四倍体鱼是可育的,而三倍体鱼是不育的.作者认为鲫鲤F2能够产生二倍体和三倍体卵子与核内复制机制和生殖细胞的融合有关.     

Sexual reproduction, hybridization, apomixis, and polyploidization in the genus Boechera (Brassicaceae)

Of the 340 genera in the Brassicaceae, apomictic reproduction is found only in the North American genus Boechera. We investigated phylogenetic relationships, ability to hybridize, mating system, and ploidy levels of 92 lines sampled from 85 populations and representing 19 Boechera species. Phylogenetic analyses based on chloroplast DNA sequences identified three lineages in the genus. Reciprocal crosses of each line were made to a common sexual diploid B. stricta tester. The resulting F(1) progeny were analyzed for the inheritance of polymorphic microsatellite loci, genome size, and seed production. Intraspecific B. stricta crosses confirmed that this species is mostly diploid and sexual. Interspecific crosses revealed many other species were diploid and sexual and could be successfully hybridized with the tester. We also found obligate and facultative apomictic diploid and triploid lines. De novo F(1) polyploids (either triploids or tetraploids) were derived from the union of nonreduced (from an apomictic parent) and reduced (from the tester) gametes. However, seed production of these F(1) plants was generally low, suggesting a failure in the transmission of apomixis. The creation of a wide array of segregating genetic populations will facilitate future research on the evolution and inheritance of quantitative variation in Boechera.     

Effect of triploid fitness on the coexistence of diploids and tetraploids

The conditions for the coexistence of diploids, triploids and tetraploids in a single population were investigated with a deterministic model under the assumptions that diploids might produce 2 n gametes, and that triploids had a lower fitness than other cytotypes and generated equal proportions of haploid and diploid gametes. When diploids produced only haploid gametes, the dynamics of the cytotypes were similar to that of heterozygote disadvantage with two alleles at a single locus, with triploids being equivalent to the heterozygotes. Production of 2 n gametes by diploids increased the pool of diploid gametes and created a stable equilibrium involving a majority of diploids and a minority of polyploids. When the fitness of tetraploids was equal to or higher than that of diploids, increased triploid fitness decreased the threshold of 2 n gametes necessary to deterministically fix tetraploids in the population. Conversely, when tetraploids were less fit than diploids, the rate of 2 n gamete production leading to the exclusion of diploids first decreases and then increased with increasing triploid fitness. Triploids are repeatedly found in diploid-tetraploid hybridizations and are rarely totally sterile. They might play a determinant role in the future of multiple cytotype populations. The effect of triploids depends on the relative fitness of diploids and tetraploids and is also a function of their fitness.     

Comparative cyto-embryological investigations of sexual and apomictic dandelions (Taraxacum) and their apomictic hybrids

. In the autonomous apomictic Taraxacum officinale (common dandelion), parthenogenetic egg cells develop into embryos and central cells into endosperm without prior fertilisation. Unreduced (2n) megaspores are formed via meiotic diplospory, a nonreductional type of meiosis. In this paper, we describe the normal developmental pathways of sexual and apomictic reproduction and compare these with the development observed in the apomictic hybrids. In sexual diploids, a standard type of megasporogenesis and embryo sac development is synchronised between florets in individual capitula. In contrast, we observed that megasporogenesis and gametogenesis proceeded asynchronously between florets within a single capitulum of natural triploid apomicts. In addition, autonomous endosperm and embryo development initiated independently within individual florets. Parthenogenetic initiation of embryo development in outdoor apomicts was found to be temperature-dependent. Egg cells produced in natural apomicts were not fertilised after pollination with haploid pollen grains although pollen tubes were observed to grow into their embryo sacs. Both reductional and diplosporous megasporogenesis were observed in individual inflorescences of triploid apomictic hybrids. Embryo and endosperm development initiated independently in natural and hybrid apomicts.