Competition dynamics in long‐term propagations of Schizosaccharomyces pombe strain communities

Experimental evolution studies with microorganisms such as bacteria and yeast have been an increasingly important and powerful tool to draw long‐term inferences of how microbes interact. However, while several strains of the same species often exist in natural environments, many ecology and evolution studies in microbes are typically performed with isogenic populations of bacteria or yeast. In the present study, we firstly perform a genotypic and phenotypic characterization of two laboratory and eight natural strains of the yeast Schizosaccharomyces pombe. We then propagated, in a rich resource environment, yeast communities of 2, 3, 4, and 5 strains for hundreds of generations and asked which fitness‐related phenotypes—maximum growth rate or relative competitive fitness—would better predict the outcome of a focal strain during the propagations. While the strain''s growth rates would wrongly predict long‐term coexistence, pairwise competitive fitness with a focal strain qualitatively predicted the success or extinction of the focal strain by a simple multigenotype population genetics model, given the initial community composition. Interestingly, we have also measured the competitive fitness of the ancestral and evolved communities by the end of the experiment (≈370 generations) and observed frequent maladaptation to the abiotic environment in communities with more than three members. Overall, our results aid establishing pairwise competitive fitness as good qualitative measurement of long‐term community composition but also reveal a complex adaptive scenario when trying to predict the evolutionary outcome of those communities.     

An inclusive fitness analysis of synergistic interactions in structured populations

We study the evolution of a pair of competing behavioural alleles in a structured population when there are non-additive or ‘synergistic’ fitness effects. Under a form of weak selection and with a simple symmetry condition between a pair of competing alleles, Tarnita et al. provide a surprisingly simple condition for one allele to dominate the other. Their condition can be obtained from an analysis of a corresponding simpler model in which fitness effects are additive. Their result uses an average measure of selective advantage where the average is taken over the long-term—that is, over all possible allele frequencies—and this precludes consideration of any frequency dependence the allelic fitness might exhibit. However, in a considerable body of work with non-additive fitness effects—for example, hawk–dove and prisoner''s dilemma games—frequency dependence plays an essential role in the establishment of conditions for a stable allele-frequency equilibrium. Here, we present a frequency-dependent generalization of their result that provides an expression for allelic fitness at any given allele frequency p. We use an inclusive fitness approach and provide two examples for an infinite structured population. We illustrate our results with an analysis of the hawk–dove game.     

Developmental Stability of DROSOPHILA MELANOGASTER under Artificial and Natural Selection in Constant and Fluctuating Environments

Populations of Drosophila melanogaster in constant 25° and fluctuating 20/29° environments showed increases in developmental stability, indicated by decreases in bilateral asymmetry of sterno-pleural chaeta number. In both environments, rates of decrease in asymmetry were greater under natural selection (control lines) than under artificial stabilizing selection. Overall mean asymmetry was greater in the fluctuating environment.—There was no evidence that decreased asymmetry was due to heterozygosity, and the decline in asymmetry was not explained by the decline in chaeta number in the lines under only natural selection. However, the decline was consistent with changes in total phenotypic variance and environmental variance.—The divergence between lines after 39 generations of selection was seen in differences in asymmetry and also in the genotype-environment interaction expressed in cross-culturing experiments.     

The distribution of fitness effects of new beneficial mutations in Pseudomonas fluorescens

Theoretical studies of adaptation emphasize the importance of understanding the distribution of fitness effects (DFE) of new mutations. We report the isolation of 100 adaptive mutants—without the biasing influence of natural selection—from an ancestral genotype whose fitness in the niche occupied by the derived type is extremely low. The fitness of each derived genotype was determined relative to a single reference type and the fitness effects found to conform to a normal distribution. When fitness was measured in a different environment, the rank order changed, but not the shape of the distribution. We argue that, even with detailed knowledge of the genetic architecture underpinning the adaptive types (as is the case here), the DFEs remain unpredictable, and we discuss the possibility that general explanations for the shape of the DFE might not be possible in the absence of organism-specific biological details.     

The ecology and genetics of fitness in Chlamydomonas. XIII. Fitness of long-term sexual and asexual populations in benign environments

We measured the mean fitness of populations of Chlamydomonas reinhardtii maintained in the laboratory as obligately sexual or asexual populations for about 100 sexual cycles and about 1000 asexual generations. Sexuality (random gamete fusion followed by meiosis) is expected to reduce mutational load and increase mean fitness by combining deleterious mutations from different lines of descent. We found no evidence for this process of mutation clearance: the mean fitness of sexual populations did not exceed that of asexual populations, whether measured through competition or in pure culture. We found instead that sexual progeny suffer an immediate loss in fitness, and that sexual lines maintain genetic variance for fitness. We suggest that sexual populations at equilibrium with selection in a benign environment may be mixtures of several or many epistatic genotypes with nearly equal fitness. Recombination between these genotypes reduces mean fitness and creates genetic variance for fitness. This may provide fuel for continued selection should the environment change.     

Adaptive and nonadaptive plasticity in changing environments: Implications for sexual species with different life history strategies

Populations adapt to novel environmental conditions by genetic changes or phenotypic plasticity. Plastic responses are generally faster and can buffer fitness losses under variable conditions. Plasticity is typically modeled as random noise and linear reaction norms that assume simple one‐to‐one genotype–phenotype maps and no limits to the phenotypic response. Most studies on plasticity have focused on its effect on population viability. However, it is not clear, whether the advantage of plasticity depends solely on environmental fluctuations or also on the genetic and demographic properties (life histories) of populations. Here we present an individual‐based model and study the relative importance of adaptive and nonadaptive plasticity for populations of sexual species with different life histories experiencing directional stochastic climate change. Environmental fluctuations were simulated using differentially autocorrelated climatic stochasticity or noise color, and scenarios of directional climate change. Nonadaptive plasticity was simulated as a random environmental effect on trait development, while adaptive plasticity as a linear, saturating, or sinusoidal reaction norm. The last two imposed limits to the plastic response and emphasized flexible interactions of the genotype with the environment. Interestingly, this assumption led to (a) smaller phenotypic than genotypic variance in the population (many‐to‐one genotype–phenotype map) and the coexistence of polymorphisms, and (b) the maintenance of higher genetic variation—compared to linear reaction norms and genetic determinism—even when the population was exposed to a constant environment for several generations. Limits to plasticity led to genetic accommodation, when costs were negligible, and to the appearance of cryptic variation when limits were exceeded. We found that adaptive plasticity promoted population persistence under red environmental noise and was particularly important for life histories with low fecundity. Populations producing more offspring could cope with environmental fluctuations solely by genetic changes or random plasticity, unless environmental change was too fast.     

Naturally segregating loci exhibit epistasis for fitness

The extent to which gene interaction or epistasis contributes to fitness variation within populations remains poorly understood, despite its importance to a myriad of evolutionary questions. Here, we report a multi-year field study estimating fitness of Mimulus guttatus genetic lines in which pairs of naturally segregating loci exist in an otherwise uniform background. An allele at QTL x5b—a locus originally mapped for its effect on flower size—positively affects survival if combined with one genotype at quantitative trait locus x10a (aa) but has negative effects when combined with the other genotypes (Aa and AA). The viability differences between genotypes parallel phenotypic differences for the time and node at which a plant flowers. Viability is negatively correlated with fecundity across genotypes, indicating antagonistic pleiotropy for fitness components. This trade-off reduces the genetic variance for total fitness relative to the individual fitness components and thus may serve to maintain variation. Additionally, we find that the effects of each locus and their interaction often vary with the environment.     

Hamilton's inclusive fitness in finite-structured populations

Hamilton''s formulation of inclusive fitness has been with us for 50 years. During the first 20 of those years attention was largely focused on the evolutionary trajectories of different behaviours, but over the past 20 years interest has been growing in the effect of population structure on the evolution of behaviour and that is our focus here. We discuss the evolutionary journey of the inclusive-fitness effect over this epoch, nurtured as it was in an essentially homogeneous environment (that of ‘transitive’ structures) having to adapt in different ways to meet the expectations of heterogeneous structures. We pay particular attention to the way in which the theory has managed to adapt the original constructs of relatedness and reproductive value to provide a formulation of inclusive fitness that captures a precise measure of allele-frequency change in finite-structured populations.     

Rapid fitness recovery in mutationally degraded lines of Caenorhabditis elegans

Abstract Deleterious mutation accumulation has been implicated in many biological phenomena and as a potentially significant threat to human health and the persistence of small populations. The vast majority of mutations with effects on fitness are known to be deleterious in a given environment, and their accumulation results in mean population fitness decline. However, whether populations are capable of recovering from negative effects of prolonged genetic bottlenecks via beneficial or compensatory mutation accumulation has not previously been tested. To address this question, long-term mutation-accumulation lines of the nematode Caenorhabditis elegans , previously propagated as single individuals each generation, were maintained in large population sizes under competitive conditions. Fitness assays of these lines and comparison to parallel mutation-accumulation lines and the ancestral control show that, while the process of fitness restoration was incomplete for some lines, full recovery of mean fitness was achieved in fewer than 80 generations. Several lines of evidence indicate that this fitness restoration was at least partially driven by compensatory mutation accumulation rather than a result of a generic form of laboratory adaptation. This surprising result has broad implications for the influence of the mutational process on many issues in evolutionary and conservation biology.     

Chromosome Interactions in DROSOPHILA MELANOGASTER. II. Total Fitness

In a large experiment, using nearly 200 population cages, we have measured the fitness of Drosophila melanogaster homozygous (1) for the second chromosome, (2) for the third chromosome, and (3) for both chromosomes. Twentyfour second chromosomes and 24 third chromosomes sampled from a natural population were tested. The mean fitness of the homozygous flies is 0.081 ± 0.014 for the second chromosome, 0.080 ± 0.017 for the third chromosome, and 0.079 ± 0.024 for both chromosomes simultaneously. Assuming that fitnesses are multiplicative (the additive fitness model makes no sense in the present case because of the large selection coefficients involved), the expected mean fitness of the homozygotes for both chromosomes is 0.0066; their observed fitness is more than ten times greater. Thus, it appears that synergistic interactions between loci are considerable; and that, consequently, the fitness function substantially departs from linearity. Two models are tentatively suggested for the fitness function: a "threshold" model and a "synergistic" model.—The experiments reported here confirm previous results showing that the concealed genetic load present in natural populations of Drosophila is sufficient to account for the selective maintenance of numerous polymorphisms (of the order of 1000).     

Mutant alleles of small effect are primarily responsible for the loss of fitness with slow inbreeding in Drosophila melanogaster.

Multilocus simulation is used to identify genetic models that can account for the observed rates of inbreeding and fitness decline in laboratory populations of Drosophila melanogaster. The experimental populations were maintained under crowded conditions for approximately 200 generations at a harmonic mean population size of Nh approximately 65-70. With a simulated population size of N = 50, and a mean selective disadvantage of homozygotes at individual loci approximately 1-2% or less, it is demonstrated that the mean effective population size over a 200-generation period may be considerably greater than N, with a ratio matching the experimental estimate of Ne/Nh approximately 1.4. The buildup of associative overdominance at electrophoretic marker loci is largely responsible for the stability of gene frequencies and the observed reduction in the rate of inbreeding, with apparent selection coefficients in favor of the heterozygote at neutral marker loci increasing rapidly over the first N generations of inbreeding to values approximately 5-10%. The observed decline in fitness under competitive conditions in populations of size approximately 50 in D. melanogaster therefore primarily results from mutant alleles with mean effects on fitness as homozygotes of sm < or = 0.02. Models with deleterious recessive mutants at the background loci require that the mean selection coefficient against heterozygotes is at most hsm approximately 0.002, with a minimum mutation rate for a single Drosophila autosome 100 cM in length estimated to be in the range 0.05-0.25, assuming an exponential distribution of s. A typical chromosome would be expected to carry at least 100-200 such mutant alleles contributing to the decline in competitive fitness with slow inbreeding.     

Host specificity of microbiome assembly and its fitness effects in phytoplankton

Insights into symbiosis between eukaryotic hosts and their microbiomes have shifted paradigms on what determines host fitness, ecology, and behavior. Questions remain regarding the roles of host versus environment in shaping microbiomes, and how microbiome composition affects host fitness. Using a model system in ecology, phytoplankton, we tested whether microbiomes are host-specific, confer fitness benefits that are host-specific, and remain conserved in time in their composition and fitness effects. We used an experimental approach in which hosts were cleaned of bacteria and then exposed to bacterial communities from natural environments to permit recruitment of microbiomes. We found that phytoplankton microbiomes consisted of a subset of taxa recruited from these natural environments. Microbiome recruitment was host-specific, with host species explaining more variation in microbiome composition than environment. While microbiome composition shifted and then stabilized over time, host specificity remained for dozens of generations. Microbiomes increased host fitness, but these fitness effects were host-specific for only two of the five species. The shifts in microbiome composition over time amplified fitness benefits to the hosts. Overall, this work solidifies the importance of host factors in shaping microbiomes and elucidates the temporal dynamics of microbiome compositional and fitness effects.Subject terms: Microbial ecology, Freshwater ecology     

Fitness,risk taking,and spatial behavior covary with boldness in experimental vole populations

Individuals of a population may vary along a pace‐of‐life syndrome from highly fecund, short‐lived, bold, dispersive “fast” types at one end of the spectrum to less fecund, long‐lived, shy, plastic “slow” types at the other end. Risk‐taking behavior might mediate the underlying life history trade‐off, but empirical evidence supporting this hypothesis is still ambiguous. Using experimentally created populations of common voles (Microtus arvalis)—a species with distinct seasonal life history trajectories—we aimed to test whether individual differences in boldness behavior covary with risk taking, space use, and fitness. We quantified risk taking, space use (via automated tracking), survival, and reproductive success (via genetic parentage analysis) in 8 to 14 experimental, mixed‐sex populations of 113 common voles of known boldness type in large grassland enclosures over a significant part of their adult life span and two reproductive events. Populations were assorted to contain extreme boldness types (bold or shy) of both sexes. Bolder individuals took more risks than shyer ones, which did not affect survival. Bolder males but not females produced more offspring than shy conspecifics. Daily home range and core area sizes, based on 95% and 50% Kernel density estimates (20 ± 10 per individual, n = 54 individuals), were highly repeatable over time. Individual space use unfolded differently for sex‐boldness type combinations over the course of the experiment. While day ranges decreased for shy females, they increased for bold females and all males. Space use trajectories may, hence, indicate differences in coping styles when confronted with a novel social and physical environment. Thus, interindividual differences in boldness predict risk taking under near‐natural conditions and have consequences for fitness in males, which have a higher reproductive potential than females. Given extreme inter‐ and intra‐annual fluctuations in population density in the study species and its short life span, density‐dependent fluctuating selection operating differently on the sexes might maintain (co)variation in boldness, risk taking, and pace‐of‐life.     

The distribution of fitness effects in an uncertain world

The distribution of fitness effects (DFE) among new mutations plays a critical role in adaptive evolution and the maintenance of genetic variation. Although fitness landscape models predict several key features of the DFE, most theory to date focuses on predictable environmental conditions, while ignoring stochastic environmental fluctuations that feature prominently in the ecology of many organisms. Here, we derive an extension of Fisher's geometric model that incorporates two common effects of environmental variation: (1) nonadaptive genotype‐by‐environment interactions (G × E), in which the phenotype of a given genotype varies across environmental contexts; and (2) random fluctuation of the fitness optimum, which generates fluctuating selection. We show that both factors cause a mismatch between the DFE within single generations and the distribution of geometric mean fitness effects (averaged over multiple generations) that governs long‐term evolutionary change. Such mismatches permit strong evolutionary constraints—despite an abundance of beneficial fitness variation within single environmental contexts—and to conflicting DFE estimates from direct versus indirect inference methods. Finally, our results suggest an intriguing parallel between the genetics and ecology of evolutionary constraints, with environmental fluctuations and pleiotropy placing qualitatively similar limits on the availability of adaptive genetic variation.     

The nature of nurture in a wild mammal's fitness

Genetic variation in fitness is required for the adaptive evolution of any trait but natural selection is thought to erode genetic variance in fitness. This paradox has motivated the search for mechanisms that might maintain a population''s adaptive potential. Mothers make many contributions to the attributes of their developing offspring and these maternal effects can influence responses to natural selection if maternal effects are themselves heritable. Maternal genetic effects (MGEs) on fitness might, therefore, represent an underappreciated source of adaptive potential in wild populations. Here we used two decades of data from a pedigreed wild population of North American red squirrels to show that MGEs on offspring fitness increased the population''s evolvability by over two orders of magnitude relative to expectations from direct genetic effects alone. MGEs are predicted to maintain more variation than direct genetic effects in the face of selection, but we also found evidence of maternal effect trade-offs. Mothers that raised high-fitness offspring in one environment raised low-fitness offspring in another environment. Such a fitness trade-off is expected to maintain maternal genetic variation in fitness, which provided additional capacity for adaptive evolution beyond that provided by direct genetic effects on fitness.     

The ecology and genetics of fitness in Chlamydomonas. IX. The rate of accumulation of variation of fitness under selection

Populations of Chlamydomonas founded by single cells were cultured in chemostats for 50 days, representing about 125 generations. The mean and variance of division rate was measured daily by withdrawing cells from the effluent and culturing them for 24 h on filtered effluent medium solidified with agar. Mean fitness did not change during the period of culture, and the behavior of neutral markers indicated that no substitutions of novel beneficial mutations occurred. However, the variance of fitness increased markedly at about the same rate in two replicate populations. The standardized rate, or mutational heritability, was Vm/VE = 4-5 x 10(-3) per generation. This is substantially greater than most other estimates for characters closely correlated with fitness. Moreover, it seems difficult to reconcile with the absence of any change in mean fitness. We investigated the possibility that frequency-dependent selection was created by spatial heterogeneity within the culture vessel by testing cell populations with different phenotypes from the top, bottom, and surface of the chemostats. However, the differentiation of these populations seemed to be attributable to phenotypic plasticity, with no evidence that their characteristics were heritable. Finally, we report an experiment in which lines were selected for about 100 generations on solid or liquid medium. These lines became specifically adapted to the medium on which they were cultured, showing that liquid and solid media, even when chemically identical, provide different conditions of growth for Chlamydomonas. The genetic variance appearing in the cultures was therefore attributed to conditionally neutral mutations that were not expressed in the chemostat. This implies that rates of accumulation of mutational variance measured in the culture environment itself (where this can be done) may greatly underestimate the variation available for a response through selection to environmental change. Moreover, it suggests that chemostat populations may be more dynamic and more diverse than is usually thought.     

Long-term experimental evolution in Escherichia coli. V. Effects of recombination with immigrant genotypes on the rate of bacterial evolution

This study builds upon an earlier experiment that examined the dynamics of mean fitness in evolving populations of Escherichia coli in which mutations were the sole source of genetic variation. During thousands of generations in a constant environment, the rate of improvement in mean fitness of these asexual populations slowed considerably from an initially rapid pace. In this study, we sought to determine whether sexual recombination with novel genotypes would reaccelerate the rate of adaption in these populations. To that end, treatment populations were propagated for an additional 1000 generations in the same environment as their ancestors, but they were periodically allowed to mate with an immigrant pool of genetically distinct Hfr (high frequency recombination) donors. These donors could transfer genes to the resident populations by conjugation, but the donors themselves could not grow in the experimental environment. Control populations were propagated under identical conditions, but in the absence of sexual recombination with the donors. All twelve control populations retained the ancestral alleles at every locus that was scored. In contrast, the sexual recombination treatment yielded dramatic increases in genetic variation. Thus, there was a profound effect of recombination on the rate of genetic change. However, the increased genetic variation in the treatment populations had no significant effect on the rate of adaptive evolution, as measured by changes in mean fitness relative to a common competitor. We then considered three hypotheses that might reconcile these two outcomes: recombination pressure, hitchhiking of recombinant genotypes in association with beneficial mutations, and complex selection dynamics whereby certain genotypes may have a selective advantage only within a particular milieu of competitors. The estimated recombination rate was too low to explain the observed rate of genetic change, either alone or in combination with hitchhiking effects. However, we documented comple x ecological interactions among some recombinant genotypes, suggesting that our method for estimating fitness relative to a common competitor might have underestimated the rate of adaptive evolution in the treatment populations.     

Temperature‐sensitive fitness cost of insecticide resistance in Chinese populations of the diamondback moth Plutella xylostella

Alleles conferring a higher adaptive value in one environment may have a detrimental impact on fitness in another environment. Alleles conferring resistance to pesticides and drugs provide textbook examples of this trade‐off as, in addition to conferring resistance to these molecules, they frequently decrease fitness in pesticide/drug‐free environments. We show here that resistance to chlorpyrifos, an organophosphate (OP), in Chinese populations of the diamondback moth, Plutella xylostella, is conferred by two mutations of ace1 – the gene encoding the acetylcholinesterase enzyme targeted by OPs – affecting the amino acid sequence of the corresponding protein. These mutations were always linked, consistent with the segregation of a single resistance allele, ace1R, carrying both mutations, in the populations studied. We monitored the frequency of ace1R (by genotyping more than 20 000 adults) and the level of resistance (through bioassays on more than 50 000 individuals) over several generations. We found that the ace1R resistance allele was costly in the absence of insecticide and that this cost was likely recessive. This fitness costs involved a decrease in fecundity: females from resistant strains laid 20% fewer eggs, on average, than females from susceptible strains. Finally, we found that the fitness costs associated with the ace1R allele were greater at high temperatures. At least two life history traits were involved: longevity and fecundity. The relative longevity of resistant individuals was affected only at high temperatures and the relative fecundity of resistant females – which was already affected at temperatures optimal for development – decreased further at high temperatures. The implications of these findings for resistance management are discussed.     

The Impact of Macroscopic Epistasis on Long-Term Evolutionary Dynamics

Genetic interactions can strongly influence the fitness effects of individual mutations, yet the impact of these epistatic interactions on evolutionary dynamics remains poorly understood. Here we investigate the evolutionary role of epistasis over 50,000 generations in a well-studied laboratory evolution experiment in Escherichia coli. The extensive duration of this experiment provides a unique window into the effects of epistasis during long-term adaptation to a constant environment. Guided by analytical results in the weak-mutation limit, we develop a computational framework to assess the compatibility of a given epistatic model with the observed patterns of fitness gain and mutation accumulation through time. We find that a decelerating fitness trajectory alone provides little power to distinguish between competing models, including those that lack any direct epistatic interactions between mutations. However, when combined with the mutation trajectory, these observables place strong constraints on the set of possible models of epistasis, ruling out many existing explanations of the data. Instead, we find that the data are consistent with a “two-epoch” model of adaptation, in which an initial burst of diminishing-returns epistasis is followed by a steady accumulation of mutations under a constant distribution of fitness effects. Our results highlight the need for additional DNA sequencing of these populations, as well as for more sophisticated models of epistasis that are compatible with all of the experimental data.     

Fluctuating natural selection accounts for the evolution of diversification bet hedging

Natural environments are characterized by unpredictability over all time scales. This stochasticity is expected on theoretical grounds to result in the evolution of ‘bet-hedging’ traits that maximize the long term, or geometric mean fitness even though such traits do not maximize fitness over shorter time scales. The geometric mean principle is thus central to our interpretation of optimality and adaptation; however, quantitative empirical support for bet hedging is lacking. Here, I report a quantitative test using the timing of seed germination—a model diversification bet-hedging trait—in Lobelia inflata under field conditions. In a phenotypic manipulation study, I find the magnitude of fluctuating selection acting on seed germination timing—across 70 intervals throughout five seasons—to be extreme: fitness functions for survival are complex and multimodal within seasons and significantly dissimilar among seasons. I confirm that the observed magnitude of fluctuating selection is sufficient to account for the degree of diversification behaviour characteristic of individuals of this species. The geometric mean principle has been known to economic theory for over two centuries; this study now provides a quantitative test of optimality of a bet-hedging trait in nature.