Trade-offs, trade-ups, and high mutational parallelism underlie microbial adaptation during extreme cycles of feast and famine.

Microbes are evolutionarily robust organisms capable of rapid adaptation to complex stress, which enables them to colonize harsh environments. In nature, microbes are regularly challenged by starvation, which is a particularly complex stress because resource limitation often co-occurs with changes in pH, osmolarity, and toxin accumulation created by metabolic waste. Often overlooked are the additional complications introduced by eventual resource replenishment, as successful microbes must withstand rapid environmental shifts before swiftly capitalizing on replenished resources to avoid invasion by competing species.

Rapid evolution of mutation rate and spectrum in response to environmental and population-genetic challenges.

Ecological and demographic factors can significantly shape the evolution of microbial populations both directly and indirectly, as when changes in the effective population size affect the efficiency of natural selection on the mutation rate. However, it remains unclear how rapidly the mutation-rate responds evolutionarily to the entanglement of ecological and population-genetic factors over time. Here, we directly assess the mutation rate and spectrum of Escherichia coli clones isolated from populations evolving in response to 1000 days of different transfer volumes and resource-replenishment intervals.

Challenges and potential solutions for studying the genetic and phenotypic architecture of adaptation in microbes.

All organisms are defined by the makeup of their DNA. Over billions of years, the structure and information contained in that DNA, often referred to as genetic architecture, have been honed by a multitude of evolutionary processes. Mutations that cause genetic elements to change in a way that results in beneficial phenotypic change are more likely to survive and propagate through the population in a process known as adaptation.

Complex Ecotype Dynamics Evolve in Response to Fluctuating Resources.

Ecotypic diversification and its associated cooperative behaviors are frequently observed in natural microbial populations whose access to resources is often sporadic. However, the extent to which fluctuations in resource availability influence the emergence of cooperative ecotypes is not fully understood. To determine how exposure to repeated resource limitation affects the establishment and long-term maintenance of ecotypes in a structured environment, we followed 32 populations of Escherichia coli evolving to either 1-day or 10-day feast/famine cycles for 900 days.

Evolutionary Dynamics of Asexual Hypermutators Adapting to a Novel Environment.

How microbes adapt to a novel environment is a central question in evolutionary biology. Although adaptive evolution must be fueled by beneficial mutations, whether higher mutation rates facilitate the rate of adaptive evolution remains unclear. To address this question, we cultured Escherichia coli hypermutating populations, in which a defective methyl-directed mismatch repair pathway causes a 140-fold increase in single-nucleotide mutation rates.

Phenotypic plasticity as a long-term memory easing readaptations to ancestral environments.

Phenotypic plasticity refers to environment-induced phenotypic changes without mutation and is present in all organisms. The role of phenotypic plasticity in organismal adaptations to novel environments has attracted much attention, but its role in readaptations to ancestral environments is understudied. To address this question, we use the reciprocal transplant approach to investigate the multitissue transcriptomes of chickens adapted to the Tibetan Plateau and adjacent lowland.

The Limits to Estimating Population-Genetic Parameters with Temporal Data.

The ability to obtain genome-wide sequences of very large numbers of individuals from natural populations raises questions about optimal sampling designs and the limits to extracting information on key population-genetic parameters from temporal-survey data. Methods are introduced for evaluating whether observed temporal fluctuations in allele frequencies are consistent with the hypothesis of random genetic drift, and expressions for the expected sampling variances for the relevant statistics are given in terms of sample sizes and numbers. Estimation methods and aspects of statistical reliability are also presented for the mean and temporal variance of selection coefficients.

Genetic Gene Expression Changes during Environmental Adaptations Tend to Reverse Plastic Changes Even after the Correction for Statistical Nonindependence.

Organismal adaptations to new environments often begin with plastic phenotypic changes followed by genetic phenotypic changes, but the relationship between the two types of changes is controversial. Contrary to the view that plastic changes serve as steppingstones to genetic adaptations, recent transcriptome studies reported that genetic gene expression changes more often reverse than reinforce plastic expression changes in experimental evolution. However, it was pointed out that this trend could be an artifact of the statistical nonindependence between the estimates of plastic and genetic phenotypic changes, because both estimates rely on the phenotypic measure at the plastic stage.

Publisher Correction: Evolutionary adaptations to new environments generally reverse plastic phenotypic changes.

The originally published HTML version of this Article contained errors in the three equations in the Methods sub-section 'Metabolic network analysis', whereby the Greek letter eta (η) was inadvertently used in place of beta (β) during the production process. These errors have now been corrected in the HTML version of the Article; the PDF was correct at the time of publication.

Evolutionary adaptations to new environments generally reverse plastic phenotypic changes.

Organismal adaptation to a new environment may start with plastic phenotypic changes followed by genetic changes, but whether the plastic changes are stepping stones to genetic adaptation is debated. Here we address this question by investigating gene expression and metabolic flux changes in the two-phase adaptation process using transcriptomic data from multiple experimental evolution studies and computational metabolic network analysis, respectively. We discover that genetic changes more frequently reverse than reinforce plastic phenotypic changes in virtually every adaptation.

Testing the neutral hypothesis of phenotypic evolution.

Although evolution by natural selection is widely regarded as the most important principle of biology, it is unknown whether phenotypic variations within and between species are mostly adaptive or neutral due to the lack of relevant studies of large, unbiased samples of phenotypic traits. Here, we examine 210 yeast morphological traits chosen because of experimental feasibility irrespective of their potential adaptive values. Our analysis is based on the premise that, under neutrality, the rate of phenotypic evolution measured in the unit of mutational size declines as the trait becomes more important to fitness, analogous to the neutral paradigm that functional genes evolve more slowly than functionless pseudogenes.

Deciphering the Genic Basis of Yeast Fitness Variation by Simultaneous Forward and Reverse Genetics.

The budding yeast Saccharomyces cerevisiae is the best studied eukaryote in molecular and cell biology, but its utility for understanding the genetic basis of phenotypic variation in natural populations is limited by inefficient association mapping due to strong and complex population structure. To overcome this challenge, we generated genome sequences for 85 strains and performed a comprehensive population genomic survey of a total of 190 diverse strains. We identified considerable variation in population structure among chromosomes and identified 181 genes that are absent from the reference genome.

Adaptive Genetic Robustness of Escherichia coli Metabolic Fluxes.

Genetic robustness refers to phenotypic invariance in the face of mutation and is a common characteristic of life, but its evolutionary origin is highly controversial. Genetic robustness could be an intrinsic property of biological systems, a result of direct natural selection, or a byproduct of selection for environmental robustness. To differentiate among these hypotheses, we analyze the metabolic network of Escherichia coli and comparable functional random networks.

The genotype-phenotype map of yeast complex traits: basic parameters and the role of natural selection.

Most phenotypic traits are controlled by many genes, but a global picture of the genotype-phenotype map (GPM) is lacking. For example, in no species do we know generally how many genes affect a trait and how large these effects are. It is also unclear to what extent GPMs are shaped by natural selection.