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Determining how adaptive possibilities do or do not become evolutionary realities is central to understanding the tempo and mode of evolutionary change. Some of the simplest evolutionary landscapes arise from underdominance at a single locus where the fitness valley consists of only one less-fit genotype. Despite their potential for rapid evolutionary change, few such examples have been investigated. We capitalized on an experimental system in which a significant evolutionary shift, the transition from uni-to-multicellularity, was observed in asexual diploid populations of Saccharomyces cerevisiae experimentally selected for increased settling rates. The multicellular phenotype results from recessive single-locus mutations that undergo loss-of-heterozygosity (LOH) events. By reconstructing the necessary heterozygous intermediate steps, we found that the evolution of multicellularity involves a decrease in size during the first steps. Heterozygous genotypes are 20% smaller in size than genotypes with functional alleles. Nevertheless, populations of heterozygotes give rise to multicellular genotypes more readily than unicellular genotypes with two functional alleles, by rapid LOH events. LOH drives adaptation that may enable rapid evolution in diploid yeast. Together these results show discordance between the phenotypic and genotypic multicellular transition. The evolutionary path to multicellularity, and the adaptive benefits of increased size, requires initial size reductions.

In order to investigate the contribution of the physical environment to variation in multicellular development of Myxococcus xanthus , phenotypes developed by different genotypes in a gradient of substrate stiffness conditions were quantitatively characterized. Statistical analysis showed that plastic phenotypes result from the genotype, the substrate conditions and the interaction between them. Also, phenotypes were expressed in two distinguishable scales, the individual and the population levels, and the interaction with the environment showed scale and trait specificity. Overall, our results highlight the constructive role of the physical context in the development of microbial multicellularity, with both ecological and evolutionary implications., Competing Interests: We have no competing interests.

Adaptive radiations are major contributors to species diversity. Although the underlying mechanisms of adaptive radiations, specialization and trade-offs, are relatively well understood, the tempo and repeatability of adaptive radiations remain elusive. Ecological specialization can occur through the expansion into novel niches or through partitioning of an existing niche. To test how the mode of resource specialization affects the tempo and repeatability of adaptive radiations, we selected replicate bacterial populations in environments that promoted the evolution of diversity either through niche expansion or through niche partitioning, and in a third low-quality single-resource environment, in which diversity was not expected to evolve. Colony size diversity evolved equally fast in environments that provided ecological opportunities regardless of the mode of resource specialization. In the low-quality environments, diversity did not consistently evolve. We observed the largest fitness improvement in the low-quality environment and the smallest the glucose-limited environment. We did not observe a change in the rate of evolutionary change in either trait or environment, suggesting that the pool of beneficial mutations was not exhausted. Overall, the mode of resource specialization did not affect the tempo or repeatability of adaptive radiations. These results demonstrate the limitations of eco-evolutionary feedbacks to affect evolutionary outcomes., (© 2015 The Author(s). Evolution © 2015 The Society for the Study of Evolution.)

The metabolic capabilities of microbes are the basis for many major biotechnological advances, exploiting microbial diversity by selection or engineering of single strains. However, there are limits to the advances that can be achieved with single strains, and attention has turned toward the metabolic potential of consortia and the field of synthetic ecology. The main challenge for the synthetic ecology is that consortia are frequently unstable, largely because evolution by constituent members affects their interactions, which are the basis of collective metabolic functionality. Current practices in modeling consortia largely consider interactions as fixed circuits of chemical reactions, which greatly increases their tractability. This simplification comes at the cost of essential biological realism, stripping out the ecological context in which the metabolic actions occur and the potential for evolutionary change. In other words, evolutionary stability is not engineered into the system. This realization highlights the necessity to better identify the key components that influence the stable coexistence of microorganisms. Inclusion of ecological and evolutionary principles, in addition to biophysical variables and stoichiometric modeling of metabolism, is critical for microbial consortia design. This review aims to bring ecological and evolutionary concepts to the discussion on the stability of microbial consortia. In particular, we focus on the combined effect of spatial structure (connectivity of molecules and cells within the system) and ecological interactions (reciprocal and non-reciprocal) on the persistence of microbial consortia. We discuss exemplary cases to illustrate these ideas from published studies in evolutionary biology and biotechnology. We conclude by making clear the relevance of incorporating evolutionary and ecological principles to the design of microbial consortia, as a way of achieving evolutionarily stable and sustainable systems.

Disentangling individual selection from kin selection is one of the greatest challenges of evolutionary biology. Even solitary organisms that do not interact directly with conspecifics may interact indirectly with them through competition for resources. As a result, traits that appear to affect individual fitness alone can also modify the fitness of relatives nearby and thus may evolve partially through these cryptic indirect fitness effects. Here we develop a method to quantitatively separate direct and indirect fitness consequences when some microbes become dormant, while neighbors of the same genotype remain active. Dormant microbes typically survive stresses that kill metabolically active cells, but dormancy also has a social side effect, sparing resources that may be used by nondormant individuals for growth. In structured populations, spared resources may be preferentially consumed by nondormant clonemates, providing an indirect benefit. Without population structure, however, exploitation by a never-dormant competitor imposes an indirect fitness cost on dormant cells. Cryptic indirect fitness effects may play a significant role in the evolution of many ostensibly asocial traits.

Multicellular complexity is a central topic in biology, but the evolutionary processes underlying its origin are difficult to study and remain poorly understood. Here we use experimental evolution to investigate the tempo and mode of multicellular adaptation during a de novo evolutionary transition to multicellularity. Multicelled "snowflake" yeast evolved from a unicellular ancestor after 7 days of selection for faster settling through liquid media. Over the next 220 days, snowflake yeast evolved to settle 44% more quickly. Throughout the experiment the clusters evolved faster settling by three distinct modes. The number of cells per cluster increased from a mean of 42 cells after 7 days of selection to 114 cells after 227 days. Between days 28 and 65, larger clusters evolved via a twofold increase in the mass of individual cells. By day 227, snowflake yeast evolved to form more hydrodynamic clusters that settle more quickly for their size than ancestral strains. The timing and nature of adaptation in our experiment suggests that costs associated with large cluster size favor novel multicellular adaptations, increasing organismal complexity., (© 2013 The Author(s). Evolution © 2013 The Society for the Study of Evolution.)

Organismal development and evolution are complex, multifaceted processes that depend intimately on context. They are subject to environmental influences, chance appearance and fixation of mutations, and numerous other idiosyncrasies. Genomics is detailing the molecular signature of effects of these mechanisms on phenotypes, but because numerous distinct evolutionary explanations can produce a given genomic pattern, the molecular details, rather than elucidating process, typically distract from explanatory insight and contribute little to predictive capability. While genomic research has burgeoned, direct study of evolutionary and developmental processes has lagged. We advocate for reinvigoration of direct study of process, along with refocusing of attention on questions of broad biological import, as more productive of urgently needed insights, which genomic approaches are not providing., (© 2012 The Author(s). Evolution© 2012 The Society for the Study of Evolution.)

Microbial communities are responsible for important ecosystem processes, and their activities are regulated by environmental factors such as temperature and solar ultraviolet radiation. Here we investigate changes in aquatic microbial community structure, diversity, and evenness in response to changes in temperature and UV radiation. For this purpose, 15 mesocosms were seeded with both microbial mat communities and plankton from natural pools within the Cuatro Cienegas Basin (Mexico). Clone libraries (16S rRNA) were obtained from water samples at the beginning and at the end of the experiment (40 days). Phylogenetic analysis indicated substantial changes in aquatic community composition and structure in response to temperature and UV radiation. Extreme treatments with elevation in temperature or UV radiation reduced diversity in relation to the Control treatments, causing a reduction in richness and increase in dominance, with a proliferation of a few resistant operational taxonomic units. Each phylum was affected differentially by the new conditions, which translates in a differential modification of ecosystem functioning. This suggests that the impact of environmental stress, at least at short term, will reshape the aquatic bacterial communities of this unique ecosystem. This work also demonstrates the possibility of designing manageable synthetic microbial community ecosystems where controlled environmental variables can be manipulated. Therefore, microbial model systems offer a complementary approach to field and laboratory studies of global research problems associated with the environment.

Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental evolution, we show that key steps in this transition could have occurred quickly. We subjected the unicellular yeast Saccharomyces cerevisiae to an environment in which we expected multicellularity to be adaptive. We observed the rapid evolution of clustering genotypes that display a novel multicellular life history characterized by reproduction via multicellular propagules, a juvenile phase, and determinate growth. The multicellular clusters are uniclonal, minimizing within-cluster genetic conflicts of interest. Simple among-cell division of labor rapidly evolved. Early multicellular strains were composed of physiologically similar cells, but these subsequently evolved higher rates of programmed cell death (apoptosis), an adaptation that increases propagule production. These results show that key aspects of multicellular complexity, a subject of central importance to biology, can readily evolve from unicellular eukaryotes.

Ultraviolet (UV) light is a major cause of stress, mutation, and mortality in microorganisms, causing numerous forms of cellular damage. Nevertheless, there is tremendous variation within and among bacterial species in their sensitivity to UV light. We investigated direct and correlated responses to selection during exposure to UV. Replicate lines of Escherichia coli K12 were propagated for 600 generations, half with UV and half as a control without UV. All lines responded to selection, and we found strong positive and negative correlated responses to selection associated with increased UV resistance. Compared to Control populations, UV-selected populations increased in desiccation and starvation resistance approximately twofold but were 10 times more sensitive to hypersalinity. There was little evidence for a persistent large competitive fitness cost to UV resistance. These results suggest that natural variation in UV resistance may be maintained by trade-offs for resistance to other abiotic sources of mortality. We observed an average twofold increase in cell size by the UV-selected populations, consistent with a structural mode of adaptation to UV exposure having preadaptive and maladaptive consequences to other abiotic stresses., (© 2011 The Author(s). Evolution© 2011 The Society for the Study of Evolution.)

At the desert oasis of Cuatro Ciénegas in Coahuila, México, more than 300 oligotrophic pools can be found and a large number of endemic species of plants and animals. The most divergent taxa of diatoms, snail and fishes are located in the Churince hydrological system, where we analyzed the local diversification of cultivable Firmicutes and Actinobacteria. The Churince hydrological system is surrounded by gypsum dunes and has a strong gradient for salinity, temperature, pH and dissolved oxygen. In August 2003, surface water samples were taken in 10 sites along the Churince system together with the respective environmental measurements. 417 thermo-resistant bacteria were isolated and DNA was extracted to obtain their BOX-PCR fingerprints, revealing 55 different patterns. In order to identify similarities and differences in the diversity of the various sampling sites, an Ordination Analysis was applied using Principal Component Analysis. This analysis showed that conductivity is the environmental factor that explains the distribution of most of the microbial diversity. Phylogenetic reconstruction from their 16S rRNA sequences was performed for a sample of 150 isolates. Only 17 sequences had a 100% match in the Gene Bank (NCBI), representing 10 well known cosmopolitan taxa. The rest of the sequences cluster in 22 clades for Firmicutes and another 22 clades for Actinobacteria, supporting the idea of high diversity and differentiation for this site.

Spatial structure has been identified as a major contributor to the maintenance of diversity. Here, we show that the impact of spatial structure on diversity is strongly affected by the ecological mechanisms maintaining diversity. In well-mixed, unstructured environments, microbial populations can diversify by production of metabolites during growth, providing additional resources for novel specialists. By contrast, spatially structured environments potentially limit such facilitation due to reduced metabolite diffusion. Using replicate microcosms containing the bacterium Escherichia coli, we predicted the loss of diversity during an environmental shift from a spatially unstructured environment to spatially structured conditions. Although spatial structure is frequently observed to be a major promoter of diversity, our results indicate that it can also have negative impacts on diversity.

Resistance to predation, herbivory, or disease often comes at a cost such that resistant genotypes are competitively inferior to their sensitive counterparts in the absence of predators, herbivores, or pathogens. The effects of this trade-off on natural populations depend on its sensitivity to environmental changes. We used Escherichia coli and bacteriophage T4 as a model predator/prey system to study the effects of temperature on the cost of resistance. An array of independent T4-resistant mutants, derived from a single ancestral strain of E. coli B, had a mean reduction in competitive fitness that depended strongly on environmental temperature; the cost of resistance generally increased with temperature. Genetic variance for fitness among phage-resistant mutants also depended on temperature; however, genetic variance increased at high and low thermal extremes. These results suggest that temperature is likely to be an important determinant of the consequences of predation in natural communities. We also discuss the underlying mechanistic basis for the cost of resistance in this system and its interaction with temperature.

Endosymbionts and their hosts have inherently ambiguous relationships as symbionts typically depend upon their hosts for shelter, nutrition, and reproduction. Endosymbionts can acquire these needs by two alternative strategies: exploitation and cooperation. Parasites exploit hosts to advance their own reproduction at the cost of host fitness. In contrast, mutualists increase their reproductive output by increasing host fitness. Very often the distinction between parasites and mutualists is not discrete but rather contingent on the environment in which the interaction occurs, and can shift along a continuous scale from parasitism to mutualism. The cost benefit dynamics at any point along this continuum are of particular interest as they establish the likelihood of an interaction persisting or breaking down. Here we show how the interaction between the yeast Saccharomyces cerevisiae and an endosymbiotic killer virus is strongly dependent on both host ploidy and environmental pH. Additionally we elucidate the mechanisms underlying the ploidy-dependent interaction. Understanding these dynamics in the short-term is key to understanding how genetic and environmental factors impact community diversity.

The ability of rare types to invade populations is important for the maintenance of diversity and spread of beneficial variants. Spatial structure promotes strategies of interference competition by limiting diffusion of interference toxins and resources, often allowing interference competitors to invade when rare. Consistent with previous results in other microbial systems, toxin production by Saccharomyces cerevisiae is advantageous in spatially structured, high-density environments, but not in unstructured environments. However, at low density and at low frequency, rare toxin producers cannot invade populations of common, sensitive, toxin nonproducers. This is because the likelihood of interaction between toxin producers and sensitives depends upon the density and frequency of both competitors.

It is generally thought that random mutations will, on average, reduce an organism's fitness because resulting phenotypic changes are likely to be maladaptive. This relationship leads to the prediction that mutations that alter more phenotypic traits, that is, are more pleiotropic, will impose larger fitness costs than mutations that affect fewer traits. Here we present a systems approach to test this expectation. Previous studies have independently estimated fitness and morphological effects of deleting all nonessential genes in Saccharomyces cerevisiae. Using datasets generated by these studies, we examined the relationship between the pleiotropic effect of each deletion mutation, measured as the number of morphological traits differing from the parental strain, and its effect on fitness. Pleiotropy explained approximately 18% of variation in fitness among the mutants even once we controlled for correlations between morphological traits. This relationship was robust to consideration of other explanatory factors, including the number of protein-protein interactions and the network position of the deleted genes. These results are consistent with pleiotropy having a direct role in affecting fitness.

Adaptive speciation has gained popularity as a fundamental process underlying the generation of diversity. We tested whether populations respond to similar forms of disruptive selection by diversifying in similar or parallel ways by investigating diversified populations of Escherichia coli B evolved in glucose and glucose-acetate environments. In both environments, the populations have differentiated into two phenotypes, named for their characteristic colony morphologies: large (L) and small (S). Each type is heritable and this polymorphism (or 'diversified pair') appears to be maintained by negative frequency dependence. The L and S phenotypes from different environments are convergent in their colony morphology and growth characteristics. We tested whether diversification was parallel by conducting competition experiments between L and S types from different environments. Our results indicate that replicate diversified pairs from different environments have not diversified in parallel ways and suggest that subtle differences in evolutionary environment can crucially affect the outcome of adaptive diversification.

Most models of speciation require gradual change and geographic or ecological isolation for new species to arise. Homoploid hybrid speciation occurred readily between Saccharomyces cerevisiae and Saccharomyces paradoxus. Hybrids had high self-fertility (about 82%), low fertility when backcrossed to either parental species (about 7.5%), and vigorous growth under different thermal environments that favored one or the other of the parental species. Extensive karyotypic changes (tetrasomy) were observed in the hybrids, although genic incompatibilities accounted for 50% of the variation in self-fertility.

Hybrid sterility is thought to be due to deleterious epistatic interactions between genes from different species. Here we demonstrate that dominant genic incompatibility does not contribute to sterility in hybrids between Saccharomyces cerevisiae and five closely related species. Sterile diploids were made fertile by genome doubling to produce hybrid tetraploids. Based on these and previous results, we conclude that neither genic incompatibility nor classical chromosomal speciation models apply.

Adaptive radiation is a fundamental process in the evolution of biodiversity. The effects of seasonality, resource partitioning, and spatial heterogeneity have been examined experimentally using evolving populations of microbes. In all environmental conditions examined, ecological interactions have large effect on the likelihood and outcome of adaptive radiation. Adaptive radiation in seasonal environments can arise because of demographic trade-offs and excretion of metabolites. Resource partitioning can occur even in the absence of temporal or spatial heterogeneity. Spatial heterogeneity arising via growth is sufficient to generate microenvironments and subsequent adaptive radiation. However, ecological interactions maintaining diversity can be sensitive to slight alterations of the environmental conditions. Laboratory populations of microbes are ideal model systems to test the factors essential for adaptive radiation.

Twelve populations of Escherichia coli were founded from a single clone and propagated for 2000 generations in identical glucose-limited environments. During this time, the mean fitnesses of the evolving populations relative to their common ancestor improved greatly, but their fitnesses relative to one another diverged only slightly. Although the populations showed similar fitness increases, they may have done so by different underlying adaptations, or they may have diverged in other respects by random genetic drift. Therefore, we examined the relative fitnesses of independently derived genotypes in two other sugars, maltose and lactose, to determine whether they were homogeneous or heterogeneous in these environments. The genetic variation among the derived lines in fitness on maltose and lactose was more than 100-times greater than their variation in fitness on glucose. Moreover, the glucose-adapted genotypes, on average, showed significant adaptation to lactose, but not to maltose. That pathways for use of maltose and glucose are virtually identical in E. coli, except for their distinct mechanisms of uptake, suggests that the derived genotypes have adapted primarily by improved glucose transport. From consideration of the number of generations of divergence, the mutation rate in E. coli, and the proportion of its genome required for growth on maltose (but not glucose), we hypothesize that pleiotropy involving the selected alleles, rather than random genetic drift of alleles at other loci, was the major cause of the variation among the derived genotypes in fitness on these other sugars., (© 1995 The Society for the Study of Evolution.)