Fitness and evolution in clonal plants: the impact of clonal growth

Seeds have often been emphasized in estimates of plant fitness because they are the units that carry genes to the next generation, disperse, and found new populations. We contend that clonal growth also needs to be considered when estimating fitness in clonal plants, regardless of whether fitness is measured from a genet or ramet perspective. Clonal growth affects genet fitness through both genet persistence and seed production. It affects ramet fitness through new ramet production, because both seeds and clonal propagants are considered offspring. The differential production of clonal propagants will contribute to fitness differences among individuals which may result in population-level changes in allele frequencies (i.e. microevolution). We describe a form of selection unique to clonal organisms, genotypic selection, that can result in evolution. Genotypic selection occurs when genotypically based traits are associated with differences in the rate of ramet production. It can lead to evolutionary change in quantitative trait means both directly and indirectly. It leads directly to change in the ramet population by increasing the proportion of ramets with more advantageous trait values. From the genet perspective, it leads indirectly to evolution within and among populations whenever significant portions of the genetic effect on a trait are inherited through seed. We argue that under most conditions, clonal growth will play a major role in the microevolution of clonal plants.     

Detecting clonemate pairs in multicellular diploid clonal species based on a shared heterozygosity index

Clonal reproduction, the formation of nearly identical individuals via mitosis in the absence of genetic recombination, is a very common reproductive mode across plants, fungi and animals. To detect clonal genetic structure, genetic similarity indices based on shared alleles are widely used, such as the Jaccard index, or identity by state. Here we propose a new pairwise genetic similarity index, the SH index, based on segregating genetic marker loci (typically single nucleotide polymorphisms) that are identically heterozygous for pairs of samples (N_SH). To test our method, we analyse two old seagrass clones (Posidonia australis, estimated to be around 8500 years old; Zostera marina, >750 years old) along with two young Z. marina clones of known age (17 years old). We show that focusing on shared heterozygosity amplifies the power to distinguish sample pairs belonging to different clones compared to methods focusing on all shared alleles. Our proposed workflow can successfully detect clonemates at a location dominated by a single clone. When the collected samples involve two or more clones, the SH index shows a clear gap between clonemate pairs and interclone sample pairs. Ideally N_SH should be on the order of approximately ≥3000, a number easily achievable via restriction-site associated DNA (RAD) sequencing or whole-genome resequencing. Another potential application of the SH index is to detect possible parent–descendant pairs under selfing. Our proposed workflow takes advantage of the availability of the larger number of genetic markers in the genomic era, and improves the ability to distinguish clonemates from nonclonemates in multicellular diploid clonal species.     

Heavy metals modify costs of reproduction and clonal growth in the stoloniferous herb Potentilla anserina

We examined costs of sexual reproduction and clonal propagation, and their consequences for resource allocation in the clonal stoloniferous herb, Potentilla anserina, a typical pioneer species in disturbed areas. We used heavy-metal treatment in soil to create unfavourable growing conditions, because costs of reproduction are more likely to be expressed when resources are limited. We also studied whether heavy metals affect the plasticity of clonal growth form that enables the plants to avoid poor growing conditions. Ramets collected from field were grown in a greenhouse under the heavy-metal treatment consisting of a control and two levels of heavy-metals added in soil. Clonal propagation was costly in terms of total biomass of flowering ramets. Also the costs of sexual reproduction were detected in flowering ramets. Contrary to our predictions, the costs of flower production were visible in the control but not in the heavy-metal contaminated plants. Only the flowering ramets were able to produce longer stolons under heavy-metal stress, but the stolon biomass was not affected by heavy metals. Results indicate that clonal propagation and sexual reproduction may be costly for P. anserina. However, the costs are modified by heavy-metal contamination.Co-ordinating editor: J. Tuomi     

Effects of light on the growth and clonal reproduction of Ligularia virgaurea

Ligularia virgaurea is a perennial herb that is widely distributed in the alpine meadow on the eastern Qinghai-Tibet plateau.We investigated the patterns of growth and reproduction of L.virgaurea under two contrasting levels of light conditions for two continuous growing seasons.Our results showed that the light affects on the maximum relative growth rate,the shoot weight ratio and the root weight ratio differed between the two growing seasons.L.virgaurea reproduced initially through rhizome in the second growing season,rather than sexual reproduction.The proportion of genets with clonal reproduction decreased under shaded conditions.A minimum genet size should be attained for clonal reproduction to begin under the shaded conditions.There was a positive linear relationship between clonal reproduction and genet size.Light level affected the allocation of total biomass to clonal structures,with less allocation under the full natural irradiance than under the shaded conditions.There seemed to be a trade-off between vegetative growth and clonal reproduction under the full natural irradiance,in terms of smaller relative growth rates of genets with clonal reproduction than those without clonal reproduction.L.virgaurea emphasized clonal reproduction under the full natural irradiance,while the plant emphasized vegetative growth under the shaded conditions.     

Asexual and sexual reproductive strategies in clonal plants

Most plants can reproduce both sexually and asexually (or vegetatively),and the balance between the two reproductive modes may vary widely between and within species.Extensive clonal growth may affect the evolution of life history traits in many ways.First,in some clonal species,sexual reproduction and sex ratio vary largely among populations.Variation in sexual reproduction may strongly affect plant's adaptation to local environments and the evolution of the geographic range.Second,clonal growth can increase floral display,and thus pollinator attraction,while it may impose serious constraints and evolutionary challenges on plants through geitonogamy that may strongly influence pollen dispersal.Geitonogamous pollination can bring a cost to plant fitness through both female and male functions.Some co-evolutionary interactions,therefore,may exist between the spatial structure and the mating behavior of clonal plants.Finally,a trade-off may exist between sexual reproduction and clonal growth.Resource allocation to the two reproductive modes may depend on environmental conditions,competitive dominance,life span,and genetic factors.If different reproductive modes represent adaptive strategies for plants in different environments,we expect that most of the resources should be allocated to sexual reproduction in habitats with fluctuating environmental conditions and strong competition,while clonal growth should be dominant in stable habitats.Yet we know little about the consequence of natural selection on the two reproductive modes and factors which control the balance of the two reproductive modes.Future studies should investigate the reproductive strategies of clonal plants simultaneously from both sexual and asexual perspectives.     

Asexual and sexual reproductive strategies in clonal plants

Most plants can reproduce both sexually and asexually (or vegetatively), and the balance between the two reproductive modes may vary widely between and within species. Extensive clonal growth may affect the evolution of life history traits in many ways. First, in some clonal species, sexual reproduction and sex ratio vary largely among populations. Variation in sexual reproduction may strongly affect plant’s adaptation to local environments and the evolution of the geographic range. Second, clonal growth can increase floral display, and thus pollinator attraction, while it may impose serious constraints and evolutionary challenges on plants through geitonogamy that may strongly influence pollen dispersal. Geitonogamous pollination can bring a cost to plant fitness through both female and male functions. Some co-evolutionary interactions, therefore, may exist between the spatial structure and the mating behavior of clonal plants. Finally, a trade-off may exist between sexual reproduction and clonal growth. Resource allocation to the two reproductive modes may depend on environmental conditions, competitive dominance, life span, and genetic factors. If different reproductive modes represent adaptive strategies for plants in different environments, we expect that most of the resources should be allocated to sexual reproduction in habitats with fluctuating environmental conditions and strong competition, while clonal growth should be dominant in stable habitats. Yet we know little about the consequence of natural selection on the two reproductive modes and factors which control the balance of the two reproductive modes. Future studies should investigate the reproductive strategies of clonal plants simultaneously from both sexual and asexual perspectives. Translated from Acta Phytoecologica Sinica, 2006, 20(1): 174–183 [译自: 植物生态学报]     

Fine-scale clonal structure and diversity within patches of a clone-forming dioecious shrub, Ilex leucoclada (Aquifoliaceae)

BACKGROUND AND AIMS: The mode of reproduction (sexual vs. asexual) is likely to have important effects on genetic variation and its spatial distribution within plant populations. An investigation was undertaken of fine-scale clonal structure and diversity within patches of Ilex leucoclada (a clone-forming dioecious shrub). METHODS: Six patches were selected in a 1-ha plot previously established in an old-growth beech forest. Two of the selected patches were composed predominantly of stems with male flowers (male patch), and two contained stems with predominantly female flowers (female patch). The remaining two patches contained stems with male flowers and stems with female flowers in more or less equal proportions (mixed patch). Different genets were distinguished using random amplified polymorphic DNA (RAPD) markers. KEY RESULTS: One hundred and fifty-six genets with different RAPD phenotypes were identified among 1928 stems from the six patches. Among the six patches, the male patches had the lowest clonal diversity, and the mixed patches had the highest. Distribution maps of the genets showed that they extended downhill, reflecting natural layering that occurred when stems were pressed to the ground by heavy snow. In every patch, there were a few large genets with many stems and many small genets with a few stems. CONCLUSION: The differences in clonal diversity among patches may be due to differences in seedling recruitment frequencies. The skewed distribution of genet size (defined as the number of stems per genet) within patches may be due to differences in the timing of germination, or age (with early-establishing genets having clear advantages for acquiring resources) and/or intraspecific competition.     

The role of sexual and clonal reproduction in maintaining population in Fritillaria camtschatcensis (L.) Ker-Gawl. (Liliaceae)

Fritillaria camtschatcensis can reproduce by means of both sexual reproduction and clonal multiplication. Despite prolific seed production, no seedlings have been found for several years in natural populations on Mt Hakusan. The purposes of this paper are to clarify: (i) whether population size is maintained mainly by clonal multiplication; and (ii) if this is the case, to what extent occasional seedling establishment affects population growth rate and population structure. Two permanent quadrats were placed in subalpine meadows in 1992 on Mt Hakusan. Plant size, location and reproductive states for all ramets in the quadrats were recorded every year. Projection matrices were created based on field census, and computer simulation experiments were performed. Fritillaria camtschatcensis had two types of flower, male flower and cosexual flower, and they were changeable. This is the first report on sex lability in Fritillaria. Clonal growth was more closely correlated with life-history stages, especially with sexual states than with plant size. The population growth rate, , was 1.006 for the Mizuyajiri population and 1.047 for the Nanryu population, respectively. Seedlings were found in 1996 for the first time. These facts indicate that populations of F. camtschatcensis on Mt Hakusan can usually be maintained by clonal multiplication. However, it is not yet certain whether seeds germinate every year or whether a flush of seedling emergence occurs once in every few years in natural populations. Computer simulation revealed that: (i) there was a critical germination rate above which population growth rate suddenly increased; and (ii) occasional seedling establishment could provide almost the same contribution to population growth rate as that of annual seedling establishment. These results suggest that population size can be maintained mainly by clonal multiplication, and the role of sexual reproduction lies beyond maintaining the population size in F. camtschatcensis.     

Population density and module demography in Trapa natans (Trapaceae), an annual,clonal aquatic macrophyte

The effects of population density on module demography were studied in Trapa natans L., an annual aquatic macrophyte capable of extensive clonal propagation. At low density, the floating plants produced ten times as many ramets (clonal offshoots) as those at high density. Module mortality occurred at three levels: leaf, ramet (shoot), and genet (genetic individual). There was 100-fold variation in the size of nuts containing germinable seeds. In early summer there was a highly significant linear relationship between dry mass of nuts and the total mass of ramets that each had produced. In early summer most (73–83%) of the variation in total plant biomass was attributable to variation in initial nut size. However the significance of initial nut size was diminished later in the season. The great success of the exotic weed T. natans at colonizing and monopolizing an aquatic habitat is a function of its highly productive clonal growth response to low-density conditions, combined with greater proportional allocation of biomass to reproductive structures, resulting in greatly increased nut production at low initial density. The species appears able to develop and maintain a population at extremely high density: plant buoyancy and the production of large, well-protected nuts allow rapid early growth from the sediment each year and early pre-emption of the water surface.     

Genetic basis and breeding application of clonal diversity and dual reproduction modes in polyploid Carassius auratus gibelio

A unisexual species is generally associated with polyploidy, and reproduced by a unisexual reproduction mode, such as gyno- genesis, hybridogenesis or parthenogenesis. Compared with other unisexual and polyploid species, gibel carp (Carassius au- ratus gibelio) has a higher ploidy level of hexaploid. It has undergone several successive rounds of genome polyploidy, and experienced an additional, more recent genome duplication event. More significantly, the dual reproduction modes, including gynogenesis and s...     

Genet structure and determinants of clonal structure in a temperate deciduous woodland herb, Uvularia perfoliata

1 We used isozyme variation to examine the genet structure of Uvularia perfoliata patches in gap and closed canopy habitats in a temperate deciduous forest in Maryland, USA.
2 A large patch in a gap habitat was composed of a small number of widely spread genets with many ramets, and a large number of genets with more restricted distribution and few ramets. Genets with many ramets were patchily distributed at a metre scale. Analysis of genet structure on a scale of square centimetres, however, revealed that the genets were highly intermingled with no clear boundaries between them. The presence at both scales of sampling of many genets with unique multilocus genotypes indicated continuing genet recruitment within the population.
3 In the closed canopy habitat, the patches examined were each composed of a single unique multilocus genotype, suggesting that each had developed by asexual propagation following the establishment of a single genet.
4 The clonal structure of U. perfoliata patches in both gap and closed canopy habitats therefore appears to depend on recruitment patterns of genets. Populations in closed canopy habitats are characterized by a 'waiting' strategy, in which asexual ramet production maintains populations until genet recruitment by seed production can occur under the more optimal conditions associated with canopy gaps. Extended sampling suggests that the genetic diversity of U. perfoliata populations is primarily controlled by the disturbance regime of the forest canopy.     

Sexual dimorphism in the energetics of reproduction and growth of North Sea plaice, Pleuronectes platessa L.

The chemical composition and energy content of North Sea plaice during the spawning period were examined in mature males and females and in immature fish, to study differences in the allocation of energy over reproduction and somatic growth between the sexes. At the beginning of the spawning period mature males and females had equal dry weights of lipid that were 70% higher than in immatures. Protein content in mature males was equal to that in immatures but was 23 % higher in mature females. Immature males and females did not differ in chemical composition. At the end of the spawning period, spent and immature fish had equal lipid contents, but protein content in spent females was 10% lower than in spent males, and 17% lower than in immatures. Gross energy content of the body decreased by 44% (65·2 to 36·3 J cm^-3) in mature females, 27% (55·0 to 40·OJ cm^-3) in mature males, and 9% (48·7 to 44·2J cm^-3) in immatures. Energy content of plaice eggs was estimated at 6·60 kJ per 1000 eggs. Reproductive investment was estimated from the energy loss during the spawning period and included the energy of sex products and spawning metabolism. Somatic growth comprised the annual increase in energy content of fish. The pattern of energy allocation over reproduction and somatic growth differed between males and females. Males started their reproduction at a smaller length and a younger age and allocated a higher proportion of the available energy into reproduction than females. Available energy resources for somatic growth and reproduction (surplus production) were equal between the sexes up to a length of about 30 cm. Beyond this length male surplus production levelled off whereas female surplus production continued to increase. The differences in surplus production and the allocation patterns are discussed. For female plaice the energy allocated into egg production was estimated as between 48 and 64% of the total amount of energy lost during spawning. The remaining energy is used for metabolism during the spawning period, yielding an estimate of the metabolic rate of mature females of between 6·4 and 9·1 kJ day^-1. A maximum estimate of the metabolic rate of mature males was 7·4 kJ day^-1.     

Sexual reproduction and dimorphism in the pathogenic basidiomycetes

Many fungi in the Basidiomycota have a dimorphic life cycle, where a monokaryotic yeast form alternates with a dikaryotic hyphal form. Most of the dimorphic basidiomycetes are pathogenic on plants, animals or other fungi. In these species, infection of a host appears to be closely linked to both dimorphism and the process of sexual reproduction. Sex in fungi is governed by a specialized region of the genome known as the mating type locus that confers cell-type identity and regulates progression through the sexual cycle. Here we investigate sexual reproduction and lifestyle in emerging human pathogenic yeasts and plant pathogenic smuts of the Basidiomycota and examine the relationship among sex, dimorphism and pathogenesis.     

Sex-ratio bias and clonal reproduction in the brittle star Ophiactis savignyi

Although the sex ratios of many groups conform to Fisher's (1930) prediction that parents should invest equally in daughters and sons, a number of taxa are characterized by excesses of one gender. A variety of mechanisms may lead to sex ratio biases, but in organisms that reproduce clonally as well as sexually, gender differences in the rate of cloning could drive the development of sex-ratio biases. In this study, I demonstrate that males of the clonal brittle star Ophiactis savignyi were significantly more likely to divide than females and that the magnitude of this difference was sufficient to explain the consistent and significant excess of males in natural populations. Females were significantly more likely to lose sexual reproductive capabilities following division, and this greater cost associated with division may explain why females are less likely to divide. Gender differences in mortality rates are unlikely to explain the excess of males in this species. Because of their potential influence on the operational sex ratio, gender differences in division rates may have important ecological and evolutionary implications including effects on the direction and strength of selection.