Clonal Life Research Articles

Evolutionary consequences of nascent multicellular life cycles.

A key step in the evolutionary transition to multicellularity is the origin of multicellular groups as biological individuals capable of adaptation. Comparative work, supported by theory, suggests clonal development should facilitate this transition, although this hypothesis has never been tested in a single model system. We evolved 20 replicate populations of otherwise isogenic clonally reproducing 'snowflake' yeast (Δace2/∆ace2) and aggregative 'floc' yeast (GAL1p::FLO1 /GAL1p::FLO1) with daily selection for rapid growth in liquid media, which favors faster cell division, followed by selection for rapid sedimentation, which favors larger multicellular groups. While both genotypes adapted to this regime, growing faster and having higher survival during the group-selection phase, there was a stark difference in evolutionary dynamics. Aggregative floc yeast obtained nearly all their increased fitness from faster growth, not improved group survival; indicating that selection acted primarily at the level of cells. In contrast, clonal snowflake yeast mainly benefited from higher group-dependent fitness, indicating a shift in the level of Darwinian individuality from cells to groups. Through genome sequencing and mathematical modeling, we show that the genetic bottlenecks in a clonal life cycle also drive much higher rates of genetic drift-a result with complex implications for this evolutionary transition. Our results highlight the central role that early multicellular life cycles play in the process of multicellular adaptation.

Invasive clonal plants possess greater capacity for division of labor than natives in high patch contrast environments.

Invasion success of clonal plants is closely related to their unique clonal life history, and clonal division of labor is a crucial clonal trait. However, so far, it is unclear whether invasive alien clonal species generally possess a greater capacity for division of labor than native species and whether this pattern is affected by environmental conditions. To test whether patch contrast affects the differences in the capacity for division of labor between invasive alien and native clonal plants, we selected five pairs of exotic invasive and native clonal plant species that are congeneric and co-occurring in China as experimental materials. We grew the clonal fragment pairs of these invasive and native plants under high, low, or no contrast of reciprocal patchiness of light and nutrient, respectively, with ramet connections either severed (division of labor prevented) or kept intact (division of labor allowed). The results showed that connection significantly decreased the proportion of biomass allocated to roots in distal (younger) ramets, whereas it increased in proximal (older) ramets of all studied plants under high -contrast treatments. This clear pattern strongly indicated the occurrence of division of labor. Furthermore, the connection had a more pronounced effect on the pattern of biomass allocation of invasive alien plants, resulting in a greater increase in biomass for invasive alien plants compared to native plants. These findings suggest that the invasive alien plants possess a greater capacity for division of labor, which may confer a competitive advantage to them over natives, thus facilitating their invasion success in some heterogeneous habitats such as forest edges where light and soil nutrients show a high negative correlation.

The power of observation: Eugen Warming (1918) Om Jordudløbere (‘Underground runners') and the ecology and evolution of clonal plants

Although often overlooked, the Danish botanist Eugen Warming was one the founders of ecology as a science. He also wrote extensively on plant life forms, including an essay from 1918, Om Jordudløbere (‘Underground runners'), which specifically focused on clonal plants. As was common among naturalists during the 19th century, Warming was exceptionally skillful in drawing conclusions from plain observation. The present paper examines how Warming understood and interpreted the ecology and evolution of clonal plants, and compares his insights with those emanating during the revival of research on clonal plants from the late 1970s onward. Several of the key topics in this revival were treated already by Warming, particularly clonal plants' ability of mobility by horizontal growth, the features affecting the ‘splitting' of genets into independent ramets, and how clonal life forms evolve. Despite these thematic similarities, Warming's direct impact on later research was limited, with the possible exception of the concept of plant functional types. This does not preclude that Warming's insights have bearing on the current research agenda on the ecology and evolution of clonal plants. The paper ends with a brief discussion of horizontal growth as a means to extend genet lifespan, thereby providing a basis for evolution of clonal plant life form through processes acting within genets.

Simulating life history trade-offs of clonal plants in drought

This study investigates responses of clonal plants and non-clonal plants to drought and their competition results using a spatial simulator based on clonal and nonclonal life history strategies. The clonal and non-clonal plants are designed as two phenotypes of one generic species with facultative clonal growth. Therefore, both phenotypes share the same life histories beside their allocation to aboveground and belowground growth, resulting in differences in leaf biomass, underground storage, and seed reproduction. Clonal plants tend to store biomass underground which would boost survival in the long-term, while non-clonal plants invest towards aboveground growth and thus more seed reproduction in the short-term. It is shown that allocation to storage in clonal plants provide them with an advantage when faced with severe drought since they can resprout from belowground. In comparison, non-clonal plants do better when there is no drought as they allocate more to aboveground growth and seeds. The simulations results have demonstrated how clonal life histories might impact plant population dynamics under drought, which might increase in frequency and extent as anthropogenic climate change continues. It also can be easily parameterized to investigate other species of interest under other environmental conditions.

Environmental regulation of individual body size contributes to geographic variation in clonal life cycle expression

Clonal behavior has been hypothesized to provide an escape from allometric metabolic scaling that limits the maximum mass achieved by a single individual. Here, we demonstrate the capacity of a wide-spread, non-native sea anemone to buffer its colony biomass accumulation rate across environments by modulating ramet body size through environmentally dependent growth, fission, and catabolism. In 2015, thermal reaction norms for growth and fission behavior were constructed using clonal lines of the sea anemone Diadumene lineata. In 2018, variation in growth patterns under a factorial cross of temperature level and oxygen availability was examined to test the hypothesis that individual ramet size is regulated by oxygen limitation in accordance with optimal size theory. Across a wide range of temperatures, colonies accumulated a similar amount of biomass despite a radical shift from unitary to clonal growth, supporting fission as a mechanism to buffer growth rates over a range of conditions. Individual body size appears to be regulated by the environment with increased temperature and reduced oxygen modifying fission and mass-specific growth patterns, leading to the production of smaller-bodied ramets in warm conditions. However, whether anemones in common garden conditions reduce individual body size through catabolism or fission depends on the region of origin and may relate to differences in seasonal temperature patterns among coastlines, which influence the energetic benefits of fission rate plasticity.

Characterization of a non-sexual population of Strongyloides stercoralis with hybrid 18S rDNA haplotypes in Guangxi, Southern China.

Strongyloidiasis is a much-neglected but sometimes fatal soil born helminthiasis. The causing agent, the small intestinal parasitic nematode Strongyloides stercoralis can reproduce sexually through the indirect/heterogonic life cycle, or asexually through the auto-infective or the direct/homogonic life cycles. Usually, among the progeny of the parasitic females both, parthenogenetic parasitic (females only) and sexual free-living (females and males) individuals, are present simultaneously. We isolated S. stercoralis from people living in a village with a high incidence of parasitic helminths, in particular liver flukes (Clonorchis sinensis) and hookworms, in the southern Chinese province Guangxi. We determined nuclear and mitochondrial DNA sequences of individual S. stercoralis isolated from this village and from close by hospitals and we compared these S. stercoralis among themselves and with selected published S. stercoralis from other geographic locations. For comparison, we also analyzed the hookworms present in the same location. We found that, compared to earlier studies of S. stercoralis populations in South East Asia, all S. stercoralis sampled in our study area were very closely related, suggesting a recent common source of infection for all patients. In contrast, the hookworms from the same location, while all belonging to the species Necator americanus, showed rather extensive genetic diversity even within host individuals. Different from earlier studies conducted in other geographic locations, almost all S. stercoralis in this study appeared heterozygous for different sequence variants of the 18S rDNA hypervariable regions (HVR) I and IV. In contrast to earlier investigations, except for three males, all S. stercoralis we isolated in this study were infective larvae, suggesting that the sampled population reproduces predominantly, if not exclusively through the clonal life cycles. Consistently, whole genome sequencing of individual worms revealed higher heterozygosity than reported earlier for likely sexual populations of S. stercoralis. Elevated heterozygosity is frequently associated with asexual clonal reproduction.

Clonal life style of fungi

Clonal life style of fungi

Cohesion of Clonal Life History, Senescence and Rejuvenation Induced by Autogamy of the Histophagous Ciliate Tetrahymena rostrata

The histophagous ciliate Tetrahymena rostrata was found as a parasite in the renal organs of the land snails Zonitoides nitidus and Cochlicopa lubrica. A starvation medium induced encystment, meiosis, autogamy, and development of new macronuclei. The cell division rate declined linearly with number of divisions from the last autogamy until senescence. The senescing strains were rejuvenated by further encystment-induced autogamy. It is expected, that these processes contribute to genetic variability among the local, small, and isolated T. rostrata populations. Consistent with this expectation, small divergences in the cox-1 sequences appeared even among these strains, which had been isolated from different specimens of the same host species at the same site. The divergences in this gene between our T. rostrata strains from Z. nitidus and other strains from C. lubrica, Helix aspersa, and Deroceras reticulatum in Spain (Segade et al. 2009, Parasitology 136:771-782), were beyond the limits of intra-species variability within the genus Tetrahymena. However there is the lack of inter-strain differences in the life history and cytology among our, the Spanish, and those T.rostrata strains, that are not available for "barcoding" anymore. Therefore, variability in the life history and morphology within T .rostrata is constrained by natural selection.

Searching for the best bet in life-strategy: A quantitative approach to individual performance and population dynamics in reef-building corals

Ecological signs of Earth's biosphere forewarn an alarming trajectory towards a global mass-extinction. Assessing species performance and susceptibilities to decline is essential to comprehend and reverse this trend. Yet it is challenging, given difficulties associated with quantifying individual and population processes that are variable across time, space, and life-stages. We describe a new approach to estimating and comparing species performances that combines empirical data, a novel theoretical consideration of population dynamics, and modern statistics. Our approach allows for a more realistic continuous representation of individual performances along development stages while taking into account non-linearity, and natural variability as captured by spatio-temporally replicated observations. We illustrate its application in a coral meta-assemblage composed of populations of the three major reef-building taxa Acropora, Pocillopora, Porites. Using a unique set of highly replicated observations of individual coral dynamics under various environmental conditions, we show how taxa differ in their investment in recruitment and size-specific aptitude for growth and survival, notably through different use of clonal shrinkage, fragmentation, fission, and fusion processes. Our results reveal contrasting life-history trade-offs among taxa which, along with differing patterns of density-dependent recruitment, modulate species responses to decline. These differences in coral life history traits reflect opposing life-strategies, imply regulation at differing life-stages, and explain divergence in species trajectories. Our findings indicate a high potential for resilience in Pocillopora and Porites populations, thanks respectively to a sustained recruitment that promotes demographic elasticity through replacement of individuals, and a steady resistance to mortality which confers persistence through lingering of individuals. Resilience in Acropora appears more arbitrary, given high susceptibility to perturbations and dependency of recruitment on presence of established local populations. We identify management actions that can complement Acropora's life history and benefit recovery of its populations following mortality events. Our regression-modelling approach to quantifying and comparing species performances in different population processes is applicable to all taxa, as illustrated even those with complex clonal life histories, and can be implemented at wide spatio-temporal and taxonomic coverage. It can promote more accurate representation of species dynamics in both descriptive and predictive modelling approaches. The semi-parametric contrast curve method we develop facilitates comparing response variables along continuous explicative metrics while accounting for multiple sources of complexity in empirical data. It should widely benefit investigations in ecology and quantitative science.

Induced production of brominated aromatic compounds in the alga Ceramium tenuicorne.

In the Baltic Sea, high concentrations of toxic brominated aromatic compounds have been detected in all compartments of the marine food web. A growing body of evidence points towards filamentous algae as a natural producer of these chemicals. However, little is known about the effects of environmental factors and life history on algal production of brominated compounds. In this study, several congeners of methoxylated polybrominated diphenyl ethers (MeO-PBDEs), hydroxylated polybrominated diphenyl ethers (OH-PBDEs) and brominated phenols (BPs) were identified in a naturally growing filamentous red algal species (Ceramium tenuicorne) in the Baltic Sea. The identified substances displayed large seasonal variations in the alga with a concentration peak in July. Production of MeO-/OH-PBDEs and BPs by C. tenuicorne was also established in isolated clonal material grown in a controlled laboratory setting. Based on three replicates, herbivory, as well as elevated levels of light and salinity in the culture medium, significantly increased the production of 2,4,6-tribromophenol (2,4,6-TBP). Investigation of differences in production between the isomorphic female, male and diploid clonal life stages of the alga grown in the laboratory revealed a significantly higher production of 2,4,6-TBP in the brackish water female gametophytes, compared to the corresponding marine gametophytes. Even higher concentrations of 2,4,6-TBP were produced by marine male gametophytes and sporophytes.

Functional and evolutionary analysis of the genome of an obligate fungal symbiont.

Nutritional symbionts of insects include some of the most bizarre genomes studied to date, with extremely reduced size, biased base composition, and limited metabolic abilities. A monophyletic group of aphids within the subfamily Cerataphidinae have lost the bacterial symbiont common to all other Aphididae (Buchnera aphidicola), which have been replaced by a eukaryotic one, the yeast-like symbiont (YLS). As symbionts are expected to experience reduced effective population size (Ne) and largely clonal life cycles, we used this system as a model to test the hypothesis that chronically high levels of genetic drift will result in an increase in size of a eukaryotic genome. We sequenced the genome of the YLS of the aphid Cerataphis brasiliensis and observed elevated rates of protein sequence evolution and intron proliferation in YLS orthologs relative to those of its closest-sequenced relative, consistent with predictions. A moderate amount of repetitive DNA was found along with evidence of directed mutation to prevent proliferation of repetitive elements. Despite increased intron numbers, the overall genome structure appears not to have undergone massive expansion and is around 25 Mb in size. Compared with Buchnera, the YLS appears to have a much broader metabolic repertoire, though many gene families have been reduced in the YLS relative to related fungi. The patterns observed in the YLS genome suggest that its symbiotic lifestyle is permissive to intron proliferation and accelerated sequence evolution, though other factors appear to limit its overall genome expansion.

Yeast Programed Cell Death and Aging

Yeast Programed Cell Death and Aging

Are stoneworts (Characeae) clonal plants?

Two questions have been posed: whether the concept of clonality may be applied to charophytes (Characeae) and whether species of the genus Chara differ in the features connected with clonal life strategy. The following criteria of clonality were established: 1/an iterative growth form characterised by a horizontal (above- or underground) axis and vertical (orthotropic) above-ground axes in the architecture of an individual, and 2/the ability of the upright axes to function independently and to regenerate the thallus. We determined the architecture of individuals as well as the ability of the vertical thallus fragments to continue growing and developing after separation from the parent thallus in Chara aspera, Chara globularis, Chara rudis and Chara tomentosa. It was found that both single-axis individuals and those made up of several (mostly 2–3) upright axes (branches) growing from the main horizontal axis occur in the populations of each of these species. The orthotropic axis of the thallus represents a module, a recurring structural unit. The modules, having been separated from the parent thalli, extend to form new vertical branches. However, the strategies of the species discussed in this paper vary in correspondence with differences in habitat.

Hypothesis: is yeast a clock model to study the onset of humans aging phenotypes?

In this paper we report the growth and aging of yeast colonies derived from single cells isolated by micromanipulation and seeded one by one on separated plates to avoid growth interference by surrounding colonies. We named this procedure clonal life span, and it could represent a third way of studying aging together with the replicative life span and chronological life span. In this study we observed over time the formation of cell mass similar to the human “senile warts” (seborrheic keratoses), the skin lesions that often appear after 30 years of life and increase in number and size over the years. We observed that similar signs of aging appear in yeast colonies after about 27 days of growth and increase during aging. In this respect we hypothesize to use yeast as a clock to study the onset of human aging phenotypes.

A closer look at the spatial architecture of aphid clones

Nearly 25 years ago, Ellstrand & Roose (1987) reviewed what was known at the time of the genetic structure of clonal plant species. What is the relationship between space and clonal fitness, they asked. What is the best way for a clone to grow within its ecological neighbourhood? The pot had been stirred 10 years previously by Janzen (1977), who pointed out how little we know about the population biology of clonal organisms like dandelions and aphids. He wondered whether, like good curries, outward appearances masked common ingredients. Because in no small part of the advent of molecular ecology, we know more about clonal life histories today, particularly in plants (van Dijk 2003; Vallejo-Marin et al. 2010). Surprisingly, studies of the spatial architecture of aphid clones have been comparably rare. In this issue of Molecular Ecology, Vantaux et al. characterize the finescale distribution of the black bean aphid (Aphis fabae) and in so doing, help to fill that gap. They describe a moderate degree of intermingling between aphid clones over a growing season--A. fabae clones are ‘sticky’, but only a bit. By mixing, clones directly compete with each other as well. The results of Vantaux et al. (2011) will help to integrate evolutionary patterns in aphids with the appropriate ecological scales out of which those patterns emerge.

Dynamics of distribution and performance of ramets constructing genets: a demographic–genetic study in a clonal plant, Convallaria keiskei

In clonal plants producing vegetative offspring, performance at the genet level as well as at the ramet level should be investigated in order to understand the entire picture of the population dynamics and the life history characteristics. In this study, demography, including reproduction and survival, the growth patterns and the spatial distributions of ramets within genets of the clonal herb Convallaria keiskei were explored. Vegetative growth, flowering and survival of shoots whose genets were identified using microsatellite markers were monitored in four study plots for 3 years (2003-2005). The size structures of ramets in genets and their temporal shifts were then analysed. Their spatial distributions were also examined. During the census, 274 and 149 ramets were mapped in two 1 x 2 m plots, and 83 and 94 ramets in two 2 x 2 m quadrats. Thirty-eight genotypes were identified from 580 samples. Each plot included 5-18 genets, and most ramets belonged to the predominant genet(s) in each plot. Shoots foliated yearly for several years, but flowering ramets did not have an inflorescence the next year. A considerable number of new clonal offspring persistently appeared, forming a bell-shaped curve of the size structure of ramets in each genet. Comparing the structures modelled by the normal distributions suggested variation among ramets belonging to a single genet and variation among genets. Furthermore, spatial analyses revealed clumped and distant distributions of ramet pairs in a genet, in which the distant patterns corresponded to the linearly elongating clonal growth pattern of this species. Characteristics of ramet performances such as flowering and recruitment of clonal offspring, in addition to growth, played a large part in the regulation of genet dynamics and distribution, which were different among the studied genets. These might be characteristics particularly relevant to clonal life histories.

Novel features of computer-simulated clonal life of Paramecium caudatum

The clone of the ciliated protozoan Paramecium caudatum has the immaturity period of about 60 fissions and the lifespan of about 600 fissions. These life cycle figures have been depicted through laboratory experiments that allow continuous cell divisions for hundreds, which never occur in nature. We here constructed the nature-mimicking model culture that alternated the log- and stationary phases to allow conjugation, and computer-simulated the age structure modifying parameters such as cell distributions to start the culture, fission rates, death rates, immaturity periods, probabilities of conjugation, proportions of transplantation and so on. The average and maximum ages in the culture after thousands of alternations were converged to 43±2 and 140±5 fissions, respectively, when parameters for the immaturity period and the maximum clonal lifespan were set at 60 and 600 fissions. This result explains why cells collected in nature are usually young and vigorous. The average and maximum ages proportionally prolonged as the immaturity period was prolonged, as reported true for species of the ciliate. These results indicate the validity of our simulation. The average and maximum ages remained unchanged when the initial condition for starting the culture was changed from two complementary mating-type cells to a population with a quadratic-function distribution, and when the fission rate at the log-phase and the death rate at the stationary phase were modified for older ages. The average and maximum ages changed slightly when either the conjugation rate or the proportion of transplantation was somewhat lowered. Although they changed considerably when such parameters as the immaturity period, conjugation rate and death rate were extremely modified, no clones with the age over 230 fissions appeared in any simulations. These results indicate the robustness of the model, which provides us with fresh insight into the structural system of the clonal lifespan of P. caudatum in nature.

Flooding and canopy dynamics shape the demography of a clonal Amazon understorey herb

Summary 1. Tropical forests have highly diverse and often dense understorey vegetation. However, little is known about the demography of tropical understorey species and their response to common events like flooding and gap formation that change the prevailing environmental conditions. 2. We studied the influence of flooding and canopy gaps on the demography of the widespread clonal herb Heliconia metallica in 16 populations in the Peruvian Amazon over two wet and two dry seasons. In a factorial study design, we selected several populations in canopy gaps and under a closed canopy both at flooded and non-flooded sites. 3. Using periodic matrix models, we determined projected population growth rates during seasonal and annual time intervals and applied prospective and retrospective analyses to identify the life cycle components that contributed most to the differences in annual growth rates among the four combinations of habitat conditions. 4. All populations increased in size during the wet and decreased during the dry season. In both years, projected annual growth rates of the non-flooded populations were less than 1 both in gaps and under a closed canopy. In contrast, over the 2-year study period growth rates of the flooded populations were close to 1 both in gaps and under a closed canopy. 5. The life history of H. metallica was dominated by ramet survival and clonal growth, whereas seedling recruitment was very rare. In canopy gaps, growth and clonal expansion were rapid and reproduction was frequent, whereas under a closed canopy ramets grew little and rarely flowered. Population decline at non-flooded sites was due to higher ramet mortality during the dry season. However, the effects of flooding and canopy gaps interacted and affected life-history components differently in wet and dry seasons and in successive years. 6. Synthesis . The intricate interacting effects of flooding and canopy gaps determine the population dynamics of the understorey herb H. metallica . The clonal life form and the plasticity of the ramets enable the populations to persist under variable light conditions, but may not be able to buffer the increasingly frequent periods of drought in Amazon forests.

Resource storage and the expression of clonal plant life histories

Resource storage and the expression of clonal plant life histories

A new mutation in the timing of autogamy in Paramecium tetraurelia

We have isolated a new type of Paramecium tetraurelia mutant, named rie-2, that has a long immaturity period until autogamy. We previously isolated such an autogamy mutant, designated rie-1. These two mutants had some additional common features such as dependence of the occurrence of autogamy on the temperature, involvement of a single recessive gene, lower fission rate and shorter clonal life span. However, rie-2 was considered a new type mutant distinguishable from rie-1 because of their different natures of temperature sensitivity. First, the temperature at which they resembled the wild-type phenotype was low (19 °C) in rie-2, although it was high (32 °C) in rie-1. Second, the clonal life span of rie-2 at 25 °C was similar to that of the wild-type, but it was extremely shorter at 32 °C than at 25 °C, although it was similarly shorter at both temperatures in rie-1. Third, the difference of the fission rate between mutant and wild-type was greater at 32 °C than at 25 °C in rie-2, although it was similar at both temperatures in rie-1. This report shows that a gene mutation to elongate the period until sexual maturation does not necessarily assure the long life span.