Genetic variation and the fate of beneficial mutations in asexual populations

The fate of a newly arising beneficial mutation depends on many factors, such as the population size and the availability and fitness effects of other mutations that accumulate in the population. It has proved difficult to understand how these factors influence the trajectories of particular mutations, since experiments have primarily focused on characterizing successful clones emerging from a small number of evolving populations. Here, we present the results of a massively parallel experiment designed to measure the full spectrum of possible fates of new beneficial mutations in hundreds of experimental yeast populations, whether these mutations are ultimately successful or not. Using strains in which a particular class of beneficial mutation is detectable by fluorescence, we followed the trajectories of these beneficial mutations across 592 independent populations for 1000 generations. We find that the fitness advantage provided by individual mutations plays a surprisingly small role. Rather, underlying "background" genetic variation is quickly generated in our initially clonal populations and plays a crucial role in determining the fate of each individual beneficial mutation in the evolving population.     

The influence of deleterious mutations on adaptation in asexual populations

We study the dynamics of adaptation in asexual populations that undergo both beneficial and deleterious mutations. In particular, how the deleterious mutations affect the fixation of beneficial mutations was investigated. Using extensive Monte Carlo simulations, we find that in the "strong-selection weak mutation (SSWM)" regime or in the "clonal interference (CI)" regime, deleterious mutations rarely influence the distribution of "selection coefficients of the fixed mutations (SCFM)"; while in the "multiple mutations" regime, the accumulation of deleterious mutations would lead to a decrease in fitness significantly. We conclude that the effects of deleterious mutations on adaptation depend largely on the supply of beneficial mutations. And interestingly, the lowest adaptation rate occurs for a moderate value of selection coefficient of deleterious mutations.     

Clonal interference, multiple mutations and adaptation in large asexual populations

Two important problems affect the ability of asexual populations to accumulate beneficial mutations and hence to adapt. First, clonal interference causes some beneficial mutations to be outcompeted by more-fit mutations that occur in the same genetic background. Second, multiple mutations occur in some individuals, so even mutations of large effect can be outcompeted unless they occur in a good genetic background that contains other beneficial mutations. In this article, we use a Monte Carlo simulation to study how these two factors influence the adaptation of asexual populations. We find that the results depend qualitatively on the shape of the distribution of the fitness effects of possible beneficial mutations. When this distribution falls off slower than exponentially, clonal interference alone reasonably describes which mutations dominate the adaptation, although it gives a misleading picture of the evolutionary dynamics. When the distribution falls off faster than exponentially, an analysis based on multiple mutations is more appropriate. Using our simulations, we are able to explore the limits of validity of both of these approaches, and we explore the complex dynamics in the regimes where neither one is fully applicable.     

Estimation of the rate and effect of new beneficial mutations in asexual populations

The rate and effect of available beneficial mutations are key parameters in determining how a population adapts to a new environment. However, these parameters are poorly known, in large part because of the difficulty of designing and interpreting experiments to examine the rare and intrinsically stochastic process of mutation occurrence. We present a new approach to estimate the rate and selective advantage of beneficial mutations that underlie the adaptation of asexual populations. We base our approach on the analysis of experiments that track the effect of newly arising beneficial mutations on the dynamics of a neutral marker in evolving bacterial populations and develop efficient estimators of mutation rate and selective advantage. Using extensive simulations, we evaluate the accuracy of our estimators and conclude that they are quite robust to the use of relatively low experimental replication. To validate the predictions of our model, we compare theoretical and experimentally determined estimates of the selective advantage of the first beneficial mutation to fix in a series of ten replicate populations. We find that our theoretical predictions are not significantly different from experimentally determined selection coefficients. Application of our method to suitably designed experiments will allow estimation of how population evolvability depends on demographic and initial fitness parameters.     

Biogeography of sexual and asexual populations in Bostrychia moritziana (Rhodomelaceae, Rhodophyta)

Bostrychia moritziana (Sonder ex Kützing) J. Agardh is recorded from many regions around the world. Our laboratory culture investigations have verified a sexual life cycle in isolates from Australia, Venezuela, Colombia, South Africa, Fiji, New Zealand and Indonesia. By contrast, asexual isolates producing successive generations of tetrasporophytes in laboratory culture and, presumably, in the field, are known from Australia. New Caledonia and Japan. In Australia, asexual reproduction is absent only in Victoria. In Western Australia, Northern Territory and Queensland, 99% of the isolates have asexual reproduction. In New South Wales (NSW), asexual and sexual populations are often intermixed. Of the 176 worldwide field collections, 58% were vegetative, 39% were tetrasporic, 2% were female and 1% were male. After several years of observations on the asexual isolates in culture, at least 30 successive asexual tetrasporophytic generations have developed. Only two asexual isolates (3558 and 3575) from NSW have formed a single male and female gametophyte in culture. In a self-cross of 3568, the carpospores developed into tetrasporophytes that recycled asexually. All outcrosses done with normal sexual isolates produced normal carposporophytes and the carpospores developed into tetrasporophytes that also recycled asexually. Asexual populations may arise repeatedly by loss of meiosis in tetrasporangia of sexual populations. Asexual reproduction apparently does not diminish the overall dispersal and abundance in the field. Our present bio-geographic data show that sexually reproducing popuiations of B. moritziana occur worldwide, while asexuaily reproducing populations are confined to the western Pacific. Bostrychia bispora West et Zuccarello, initially described on the basis of its asexual reproduction to distinguish it from B, moritziana, is now reduced to synonymy with B. moritziana.     

Genetic variation of geminiviruses: comparison between sexual and asexual host plant populations

One of the most promising hypotheses for the evolution of sex is that sexual reproduction is advantageous because it increases the rate of adaptive evolution in response to parasites. To investigate this advantage of sex, we compared genetic variation of geminiviruses infecting sexual and asexual populations of Eupatorium (Asteraceae). The infection frequency was 37.5% in the sexual population and 87.8% in the asexual population. The lower infection frequency in the sexual population might be the result of higher genetic diversity of host plants. If geminiviruses have diverged to counter defence systems of genetically variable hosts, genetic diversity of viruses is expected to be higher in sexual host populations than in asexual host populations. To test this expectation, we used single-strand conformation polymorphism (SSCP) analysis to examine genetic diversity of the geminiviruses in a DNA region containing the open-reading frame (ORF) C4 gene, which is known to function as a host range determinant. As predicted, higher genetic diversity of viruses was observed in the sexual population: three SSCP types were found in the asexual population while six types were found in the sexual population. Sequencing of the polymerase chain reaction (PCR) products revealed further genetic diversity. Phylogenetic analysis of the sequences showed that the SSCP types belonged to four different clades. Several SSCP types from the same clade were found in the sexual population, whereas the asexual population included only one SSCP type from each clade. Amino acid replacements of ORF C4 are suggested to be accelerated in the sexual population. This evidence supports the hypothesis that sexual reproduction is advantageous as a defence against epidemic disease.     

Spatial structure inhibits the rate of invasion of beneficial mutations in asexual populations

Populations in spatially structured environments may be divided into a number of (semi-) isolated subpopulations due to limited offspring dispersal. Limited dispersal and, as a consequence, local competition could slow down the invasion of fitter mutants, allowing the short-term coexistence of ancestral genotypes and mutants. We determined the rate of invasion of beneficial mutants of Escherichia coli, dispersed to different degrees in a spatially structured environment during 40 generations, experimentally and theoretically. Simulations as well as experimental data show a decrease in the rate of invasion with increasingly constrained dispersal. When a beneficial mutant invades from a single spot, competition with the ancestral genotype takes place only along the edges of the growing colony patch. As the colony grows, the fitness of the mutant will decrease due to a decrease in the mutant's fraction that effectively competes with the surrounding ancestor. Despite its inherently higher competitive ability, increased intragenotype competition prevents the beneficial mutant from rapidly taking over, causing short-term coexistence of superior and inferior genotypes.     

Population structure and diversity in sexual and asexual populations of the pathogenic fungus Melampsora lini

Many pathogens undergo both sexual and asexual reproduction to varying degrees, yet the ecological, genetic and evolutionary consequences of different reproductive strategies remain poorly understood. Here we investigate the population genetic structure of wild populations of the plant pathogen Melampsora lini on its host Linum marginale , using amplified fragment length polymorphism (AFLP) markers, two genes underlying pathogen virulence, and phenotypic variation in virulence. In Australia, M. lini occurs as two genetically and geographically divergent lineages (AA and AB), one of which is completely asexual (AB), and the other able to reproduce both clonally and sexually (AA). To quantify the genetic and evolutionary consequences of these different life histories, we sampled five populations in each of two biogeographical regions. Analysis of AFLP data obtained for 275 isolates revealed largely disjunct geographical distributions for the two different lineages, low genetic diversity within lineages, and strong genetic structure among populations within each region. We also detected significant divergence among populations for both Avr genes and virulence phenotypes, although generally these values were lower than those obtained with AFLP markers. Furthermore, isolates belonging to lineage AA collectively harboured significantly higher genotypic and phenotypic diversity than lineage AB isolates. Together these results illustrate the important roles of reproductive modes and geographical structure in the generation and maintenance of virulence diversity in populations of M. lini .     

Diversification in sexual and asexual organisms

Abstract Sexual reproduction has long been proposed as a major factor explaining the existence of species and species diversity. Yet, the importance of sex for diversification remains obscure because of a lack of critical theory, difficulties of applying universal concepts of species and speciation, and above all the scarcity of empirical tests. Here, we use genealogical theory to compare the relative tendency of strictly sexual and asexual organisms to diversify into discrete genotypic and morphological clusters. We conclude that asexuals are expected to display discrete clusters similar to those found in sexual organisms. Whether sexuals or asexuals display stronger clustering depends on a number of factors, but in at least some scenarios asexuals should display a stronger pattern. Confounding factors aside, the only explanation we identify for stronger patterns of diversification in sexuals than asexuals is if the faster rates of adaptive change conferred by sexual reproduction promote greater clustering. Quantitative comparisons of diversification in related sexual and asexual taxa are needed to resolve this issue. The answer should shed light not only on the importance of the different stages leading to diversification, but also on the adaptive consequences of sex, still largely unexplored from a macroevolutionary perspective.     

Accumulation of deleterious mutations in small abiotic populations of RNA

The accumulation of slightly deleterious mutations in populations leads to the buildup of a genetic load and can cause the extinction of populations of small size. Mutation-accumulation experiments have been used to study this process in a wide variety of organisms, yet the exact mutational underpinnings of genetic loads and their fitness consequences remain poorly characterized. Here, we use an abiotic system of RNA populations evolving continuously in vitro to examine the molecular events that can instigate a genetic load. By tracking the fitness decline of ligase ribozyme populations with bottleneck sizes between 100 and 3000 molecules, we detected the appearance and subsequent fixation of both slightly deleterious mutations and advantageous mutations. Smaller populations went extinct in significantly fewer generations than did larger ones, supporting the notion of a mutational meltdown. These data suggest that mutation accumulation was an important evolutionary force in the prebiotic RNA world and that mechanisms such as recombination to ameliorate genetic loads may have been in place early in the history of life.     

Allelic and genotypic diversity in long-term asexual populations of the pea aphid, Acyrthosiphon pisum in comparison with sexual populations

Many aphid species exhibit geographical variation in the mode of reproduction that ranges from cyclical parthenogenesis with a sexual phase to obligate parthenogenesis (asexual reproduction). Theoretical studies predict that organisms reproducing asexually should maintain higher allelic diversity per locus but lower genotypic diversity than organisms reproducing sexually. To corroborate this hypothesis, we evaluated genotypic and allelic diversities in the sexual and asexual populations of the pea aphid, Acyrthosiphon pisum (Harris). Microsatellite analysis revealed that populations in central Japan are asexual, whereas populations in northern Japan are obligatorily sexual. No mixed populations were detected in our study sites. Phylogenetic analysis using microsatellite data and mitochondrial cytochrome oxidase subunit I (COI) gene sequences revealed a long history of asexuality in central Japan and negated the possibility of the recent origin of the asexual populations from the sexual populations. Asexual populations exhibited much lower genotypic diversity but higher allelic richness per locus than did sexual populations. Asexual populations consisted of a few predominant clones that were considerably differentiated from one another. Sexual populations on alfalfa, an exotic plant in Japan, were most closely related to asexual populations associated with Vicia sativa L. The alfalfa-associated sexual populations harboured one COI haplotype that was included in the haplotype clade of the asexual populations. Available evidence suggests that the sexuality of the alfalfa-associated populations has recently been restored through the northward migration and colonization of alfalfa by V. sativa- associated lineages. Therefore, our results support the theoretical predictions and provide a new perspective on the origin of sexual populations.     

Rapid local adaptation in both sexual and asexual invasive populations of monkeyflowers (Mimulus spp.)

Background and AimsTraditionally, local adaptation has been seen as the outcome of a long evolutionary history, particularly with regard to sexual lineages. By contrast, phenotypic plasticity has been thought to be most important during the initial stages of population establishment and in asexual species. We evaluated the roles of adaptive evolution and phenotypic plasticity in the invasive success of two closely related species of invasive monkeyflowers (Mimulus) in the UK that have contrasting reproductive strategies: M. guttatus combines sexual (seeds) and asexual (clonal growth) reproduction while M. × robertsii is entirely asexual.MethodsWe compared the clonality (number of stolons), floral and vegetative phenotype, and phenotypic plasticity of native (M. guttatus) and invasive (M. guttatus and M. × robertsii) populations grown in controlled environment chambers under the environmental conditions at each latitudinal extreme of the UK. The goal was to discern the roles of temperature and photoperiod on the expression of phenotypic traits. Next, we tested the existence of local adaptation in the two species within the invasive range with a reciprocal transplant experiment at two field sites in the latitudinal extremes of the UK, and analysed which phenotypic traits underlie potential local fitness advantages in each species.Key ResultsPopulations of M. guttatus in the UK showed local adaptation through sexual function (fruit production), while M. × robertsii showed local adaptation via asexual function (stolon production). Phenotypic selection analyses revealed that different traits are associated with fitness in each species. Invasive and native populations of M. guttatus had similar phenotypic plasticity and clonality. M. × robertsii presents greater plasticity and clonality than native M. guttatus, but most populations have restricted clonality under the warm conditions of the south of the UK.ConclusionsThis study provides experimental evidence of local adaptation in a strictly asexual invasive species with high clonality and phenotypic plasticity. This indicates that even asexual taxa can rapidly (<200 years) adapt to novel environmental conditions in which alternative strategies may not ensure the persistence of populations.     

Mutation accumulation and fitness effects in hybridogenetic populations: a comparison to sexual and asexual systems

Background  

Female only unisexual vertebrates that reproduce by hybridogenesis show an unusual genetic composition. They are of hybrid origin but show no recombination between the genomes of their parental species. Instead, the paternal genome is discarded from the germline prior to meiosis, and gametes (eggs only) contain solely unrecombined maternal genomes. Hence hybridogens only transmit maternally inherited mutations. Hybridity is restored each generation by backcrossing with males of the sexual parental species whose genome was eliminated. In contrast, recombining sexual species propagate an intermixed pool of mutations derived from the maternal and paternal parts of the genome. If mutation rates are lower in female gametes than males, it raises the possibility for lower mutation accumulation in a hybridogenetic population, and consequently, higher population fitness than its sexual counterpart.     

Comparison of parasite communities in native and introduced populations of sexual and asexual mollies of the genus Poecilia

The parasite communities of two molly species, the sexual Poecilia latipinna and the clonal Poecilia formosa , were investigated in four populations using a novel method applicable under field conditions. In two native populations from south Texas and two introduced populations from central Texas, four species of microparasites and eight species of macroparasites were recorded. Virtually no differences in the parasite diversity and species composition could be detected between the populations. Mollies from south Texas had a higher individual parasitization index of macroparasites. There was a negative correlation between the relative number of oocytes in gravid females and their individual macroparasite load.     

Limits to adaptation in asexual populations

In asexual populations, the rate of adaptation is basically limited by the frequency and properties of spontaneous beneficial mutations. Hence, knowledge of these mutational properties and how they are affected by particular evolutionary conditions is a precondition for understanding the process of adaptation. Here, we address how the rate of adaptation of asexual populations is limited by its population size and mutation rate, as well as by two factors affecting the fraction of mutations that confer a benefit, i.e. the initial adaptedness of the population and the variability of the environment. These factors both influence which mutations are likely to occur, as well as the probability that they will ultimately contribute to adaptation. We attempt to separate the consequences of these basic population features in terms of their effect on the rate of adaptation by using results from evolution experiments with microorganisms.     

The accumulation of mutations in asexual populations and the structure of genealogical trees in the presence of selection

We study the accumulation of unfavourable mutations in asexual populations by the process of Muller's ratchet, and the consequent inevitable decrease in fitness of the population. Simulations show that it is mutations with only moderate unfavourable effect that lead to the most rapid decrease in fitness. We measure the number of fixations as a function of time and show that the fixation rate must be equal to the ratchet rate once a steady state is reached. Large bursts of fixations are observed to occur simultaneously. We relate this to the structure of the genealogical tree. We derive equations relating the rate of the ratchet to the moments of the distribution of the number of mutations k per individual. These equations interpolate between the deterministic limit (an infinite population with selection present) and the neutral limit (a finite size population with no selection). Both these limits are exactly soluble. In the neutral case, the distribution of k is shown to be non-self-averaging, i.e. the fluctuations remain very large even for very large populations. We also consider the strong-selection limit in which only individuals in the fittest surviving class have offspring. This limit is again exactly soluble. We investigate the structure of the genealogical tree relating individuals in the same population, and consider the probability (T) that two individuals had their latest common ancestor T generations in the past. The function (T) is exactly calculable in the neutral limit and the strong-selection limit, and we obtain an empirical solution for intermediate selection strengths.     

The role of sexual and asexual reproduction in structuring high latitude populations of the reef coral Pocillopora damicornis

The genotypic composition of populations of the asexually viviparous coral Pocillopora damicornis varies in a manner that challenges classical models of the roles of sexual and asexual reproduction. On the geographically isolated Hawaiian reefs and high latitude reefs in Western Australia, P. damicornis populations are highly clonal although it has been argued that sexual reproduction via broadcast spawning generates widely dispersed colonists. In contrast, on eastern Australia's tropical Great Barrier Reef populations show little evidence of clonality. Here, we compare the genotypic diversity of adult and juvenile colonies of P. damicornis at seven sites on eastern Australia's high latitude Lord Howe Island reefs to determine if levels of clonality vary with habitat heterogeneity and age of colonies (as predicted by theory) or alternatively if clonality is again always high as for other isolated reef systems. We found 55-100% of the genotypic diversity expected for random mating at all seven sites and little evidence of asexual recruitment irrespective of habitat heterogeneity (sheltered versus wave exposed) or colony age. We found reduced levels of genetic diversity compared with tropical reefs (2.75 versus 4 alleles/locus), which supports earlier findings that Lord Howe Island is an isolated reef system. Furthermore, heterozygote deficits coupled with significant genetic subdivision among sites (FST=0.102+/-0.03) is typical of populations that have limited larval connections and are inbred. We conclude that the genetic structure of P. damicornis at Lord Howe Island reflects populations that are maintained through localised recruitment of sexually produced larvae.     

Beneficial mutations, hitchhiking and the evolution of mutation rates in sexual populations

Natural selection acts in three ways on heritable variation for mutation rates. A modifier allele that increases the mutation rate is (i) disfavored due to association with deleterious mutations, but is also favored due to (ii) association with beneficial mutations and (iii) the reduced costs of lower fidelity replication. When a unique beneficial mutation arises and sweeps to fixation, genetic hitchhiking may cause a substantial change in the frequency of a modifier of mutation rate. In previous studies of the evolution of mutation rates in sexual populations, this effect has been underestimated. This article models the long-term effect of a series of such hitchhiking events and determines the resulting strength of indirect selection on the modifier. This is compared to the indirect selection due to deleterious mutations, when both types of mutations are randomly scattered over a given genetic map. Relative to an asexual population, increased levels of recombination reduce the effects of beneficial mutations more rapidly than those of deleterious mutations. However, the role of beneficial mutations in determining the evolutionarily stable mutation rate may still be significant if the function describing the cost of high-fidelity replication has a shallow gradient.     

Genetic architecture of sexual and asexual populations of the aphid Rhopalosiphum padi based on allozyme and microsatellite markers

Cyclical parthenogens, including aphids, are attractive models for comparing the genetic outcomes of sexual and asexual reproduction, which determine their respective evolutionary advantages. In this study, we examined how reproductive mode shapes genetic structure of sexual (cyclically parthenogenetic) and asexual (obligately parthenogenetic) populations of the aphid Rhopalosiphum padi by comparing microsatellite and allozyme data sets. Allozymes showed little polymorphism, confirming earlier studies with these markers. In contrast, microsatellite loci were highly polymorphic and showed patterns very discordant from allozyme loci. In particular, microsatellites revealed strong heterozygote excess in asexual populations, whereas allozymes showed heterozygote deficits. Various hypotheses are explored that could account for the conflicting results of these two types of genetic markers. A strong differentiation between reproductive modes was found with both types of markers. Microsatellites indicated that sexual populations have high allelic polymorphism and heterozygote deficits (possibly because of population subdivision, inbreeding or selection). Little geographical differentiation was found among sexual populations confirming the large dispersal ability of this aphid. In contrast, asexual populations showed less allelic polymorphism but high heterozygosity at most loci. Two alternative hypotheses are proposed to explain this heterozygosity excess: allele sequence divergence during long-term asexuality or hybrid origin of asexual lineages. Clonal diversity of asexual lineages of R. padi was substantial suggesting that they could have frozen genetic diversity from the pool of sexual lineages. Several widespread asexual genotypes were found to persist through time, as already seen in other aphid species, a feature seemingly consistent with the general-purpose genotype hypothesis.