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Yeasts are ubiquitous in temperate forests. While this broad habitat is well-defined, the yeasts inhabiting it and their life cycles, niches, and contributions to ecosystem functioning are less understood. Yeasts are present on nearly all sampled substrates in temperate forests worldwide. They associate with soils, macroorganisms, and other habitats and no doubt contribute to broader ecosystem-wide processes. Researchers have gathered information leading to hypotheses about yeasts' niches and their life cycles based on physiological observations in the laboratory as well as genomic analyses, but the challenge remains to test these hypotheses in the forests themselves. Here, we summarize the habitat and global patterns of yeast diversity, give some information on a handful of well-studied temperate forest yeast genera, discuss the various strategies to isolate forest yeasts, and explain temperate forest yeasts' contributions to biotechnology. We close with a summary of the many future directions and outstanding questions facing researchers in temperate forest yeast ecology. Yeasts present an exciting opportunity to better understand the hidden world of microbial ecology in this threatened and global habitat.

The genus Saccharomyces is an evolutionary paradox. On the one hand, it is composed of at least eight clearly phylogenetically delineated species; these species are reproductively isolated from each other, and hybrids usually cannot complete their sexual life cycles. On the other hand, Saccharomyces species have a long evolutionary history of hybridization, which has phenotypic consequences for adaptation and domestication. A variety of cellular, ecological, and evolutionary mechanisms are responsible for this partial reproductive isolation among Saccharomyces species. These mechanisms have caused the evolution of diverse Saccharomyces species and hybrids, which occupy a variety of wild and domesticated habitats. In this article, we introduce readers to the mechanisms isolating Saccharomyces species, the circumstances in which reproductive isolation mechanisms are effective and ineffective, and the evolutionary consequences of partial reproductive isolation. We discuss both the evolutionary history of the genus Saccharomyces and the human history of taxonomists and biologists struggling with species concepts in this fascinating genus.

Hybrid sterility maintains reproductive isolation between species by preventing them from exchanging genetic material. The genome sequences of the yeasts Saccharomyces paradoxus and Saccharomyces paradoxus have diverged by about 12%, yet they can mate and form viable diploid hybrids, which can reproduce asexually by mitosis. But these hybrids are sexually sterile: nearly all the gametes they produce by meiosis are inviable because they are aneuploid, lacking at least one essential chromosome. Chromosomes from the different species mis-segregate during hybrid meiosis due to anti-recombination; their sequences are too diverged to efficiently recombine and form crossovers. Previous methods to increase hybrid fertility by enhancing meiotic crossing over have had counteracting detrimental effects on asexual viability, due to increased mutagenesis and ectopic recombination. We were able to increase hybrid fertility 70-fold by suppressing two genes, MSH2 (YOL090W) and SGS1 (YMR190C), specifically during meiosis, whilst maintaining their mitotic expression. This confirms that anti-recombination is the principal cause of hybrid sterility. By overcoming this barrier, we were able to generate viable euploid hybrid gametes containing recombinant genomes from these two highly diverged parent species. We used this unique resource to map intrinsic Bateson-Dobzhansky-Muller incompatibilities contributing to hybrid gamete inviability. The ability to interbreed such diverged species will allow mapping of other intrinsic traits such as hybrid depression or vigour, extrinsic ecological adaptations that differentiate species, or commercially important characteristics.

Errors in meiosis can be important postzygotic barriers between different species. In Saccharomyces hybrids, chromosomal missegregation during meiosis I produces gametes with missing or extra chromosomes. Gametes with missing chromosomes are inviable, but we do not understand how extra chromosomes (disomies) influence hybrid gamete inviability. We designed a model predicting rates of missegregation in interspecific hybrid meioses assuming several different mechanisms of disomy tolerance, and compared predictions from the model to observations of sterility in hybrids between Saccharomyces yeast species. Sterility observations were consistent with the hypothesis that chromosomal missegregation causes hybrid sterility, and the model indicated that missegregation probabilities of 13-50% per chromosome can cause observed values of 90-99% hybrid sterility regardless of how cells tolerate disomies. Missing chromosomes in gametes are responsible for most infertility, but disomies may kill as many as 11% of the gametes produced by hybrids between S. cerevisiae and S. paradoxus.

The major cause of the sterility of F1 hybrids formed betweenSaccharomyces cerevisiaeandSaccharomyces paradoxusis anti-recombination. The failure of homologous chromosomes from the different species to recombine causes them to mis-segregate, resulting in aneuploid gametes, most of which are inviable. These effects of anti-recombination have previously impeded the search for other forms of incompatibility, such as negative genetic interactions (Bateson-Dobzhoansky-Muller incompatibilities). By suppressing the meiotic expression ofMSH2andSGS1, we could increase recombination and improve hybrid fertility seventy-fold. This allowed us to recover meiotic tetrads in which all four gametes were viable, ensuring that segregation had occurred properly to produce perfectly haploid, not aneuploid, recombinant hybrid gametes. We sequenced the genomes of 84 such tetrads, and discovered that some combinations of alleles from different species were significantly under-represented, indicating that there are incompatible genes contributing to reproductive isolation.

Hybridization between species can either promote or impede adaptation. But we know very little about the genetic basis of hybrid fitness, especially in nondomesticated organisms, and when populations are facing environmental stress. We made genetically variable F2 hybrid populations from two divergent Saccharomyces yeast species. We exposed populations to ten toxins and sequenced the most resilient hybrids on low coverage using ddRADseq to investigate four aspects of their genomes: 1) hybridity, 2) interspecific heterozygosity, 3) epistasis (positive or negative associations between nonhomologous chromosomes), and 4) ploidy. We used linear mixed-effect models and simulations to measure to which extent hybrid genome composition was contingent on the environment. Genomes grown in different environments varied in every aspect of hybridness measured, revealing strong genotype–environment interactions. We also found selection against heterozygosity or directional selection for one of the parental alleles, with larger fitness of genomes carrying more homozygous allelic combinations in an otherwise hybrid genomic background. In addition, individual chromosomes and chromosomal interactions showed significant species biases and pervasive aneuploidies. Against our expectations, we observed multiple beneficial, opposite-species chromosome associations, confirmed by epistasis- and selection-free computer simulations, which is surprising given the large divergence of parental genomes (∼15%). Together, these results suggest that successful, stress-resilient hybrid genomes can be assembled from the best features of both parents without paying high costs of negative epistasis. This illustrates the importance of measuring genetic trait architecture in an environmental context when determining the evolutionary potential of genetically diverse hybrid populations.

Although we understand the genetics of the laboratory model yeast Saccharomyces cerevisiae very well, we know little about the natural ecology and environment that shaped its genome. Most isolates of Saccharomyces paradoxus, the wild relative of S. cerevisiae, come from oak trees, but it is not known whether this is because oak is their primary habitat. We surveyed leaf litter in a forest in Northern Germany and found a strong correlation between isolation success of wild Saccharomyces and the proximity of the nearest oak. We compared the four most common tree genera and found Saccharomyces most frequently in oak litter. Interestingly, we show that Saccharomyces is much more abundant in oak leaf litter than on oak bark, suggesting that it grows in litter or soil rather than on the surfaces of oaks themselves. The distribution and abundance of Saccharomyces over the course of a year shows that oak leaf litter provides a stable habitat for the yeast, although there was significant tree-to-tree variation. Taken together, our results suggest that leaf litter rather than tree surfaces provide the better habitat for wild Saccharomyces, with oak being the preferred tree genus. 99.5 of all strains (633/636) isolated were S. paradoxus. © 2016 Society for Applied Microbiology and John Wiley Sons Ltd.

Increased species richness does not always cause increased ecosystem function. Instead, richness can influence individual species with positive or negative ecosystem effects. We investigated richness and function in fermenting wine, and found that richness indirectly affects ecosystem function by altering the ecological dominance of Saccharomyces cerevisiae. While S. cerevisiae generally dominates fermentations, it cannot dominate extremely species-rich communities, probably because antagonistic species prevent it from growing. It is also diluted from species-poor communities, allowing yeasts with lower functional impacts to dominate. We further investigated the impacts of S. cerevisiae and its competitors in high- and low-functioning wine communities, focusing on glucose consumption as an ecosystem function. S. cerevisiae is a keystone species because its presence converts low-functioning communities to communities with the same function as S. cerevisiae monocultures. Thus, even within the same ecosystem, species richness has both positive and negative effects on function.

SummarySex with another species can be disastrous, especially for organisms that mate only once, like yeast [1–3]. Courtship signals, including pheromones, often differ between species and can provide a basis for distinguishing between reproductively compatible and incompatible partners [4–6]. Remarkably, we show that the baker’s yeast Saccharomyces cerevisiae does not reject mates engineered to produce pheromones from highly diverged species, including species that have been reproductively isolated for up to 100 million years. To determine whether effective discrimination against mates producing pheromones from other species is possible, we experimentally evolved pheromone receptors under conditions that imposed high fitness costs on mating with cells producing diverged pheromones. Evolved receptors allowed both efficient mating with cells producing the S. cerevisiae pheromone and near-perfect discrimination against cells producing diverged pheromones. Sequencing evolved receptors revealed that each contained multiple mutations that altered the amino acid sequence. By isolating individual mutations, we identified specific amino acid changes that dramatically improved discrimination. However, the improved discrimination conferred by these individual mutations came at the cost of reduced mating efficiency with cells producing the S. cerevisiae pheromone, resulting in low fitness. This tradeoff could be overcome by simultaneous introduction of separate mutations that improved mating efficiency alongside those that improved discrimination. Thus, if mutations occur sequentially, the shape of the fitness landscape may prevent evolution of the optimal phenotype [7, 8]—offering a possible explanation for the poor discrimination of receptors found in nature.

The natural history of the model yeast Saccharomyces cerevisiae is poorly understood and confounded by domestication. In nature, S. cerevisiae and its undomesticated relative S. paradoxus are usually found on the bark of oak trees, a habitat very different from wine or other human fermentations. It is unclear whether the oak trees are really the primary habitat for wild yeast, or whether this apparent association is due to biased sampling. We use culturing and high-throughput environmental sequencing to show that S. paradoxus is a very rare member of the oak bark microbial community. We find that S. paradoxus can grow well on sterile medium made from oak bark, but that its growth is strongly suppressed when the other members of the community are present. We purified a set of twelve common fungal and bacterial species from the oak bark community and tested how each affected the growth of S. paradoxus in direct competition on oak bark medium at summer and winter temperatures, identifying both positive and negative interactions. One Pseudomonas species produces a diffusible toxin that suppresses S. paradoxus as effectively as either the whole set of twelve species together or the complete community present in nonsterilized oak medium. Conversely, one of the twelve species, Mucilaginibacter sp., had the opposite effect and promoted S. paradoxus growth at low temperatures. We conclude that, in its natural oak tree habitat, S. paradoxus is a rare species whose success depends on the much more abundant microbial species surrounding it.

Signaling peptides enable communication between cells, both within and between individuals, and are therefore key to the control of complex physiological and behavioral responses. Since their small sizes prevent direct transmission to secretory pathways, these peptides are often produced as part of a larger polyprotein comprising precursors for multiple related or identical peptides; the physiological and behavioral consequences of this unusual gene structure are not understood. Here, we show that the number of mature-pheromone-encoding repeats in the yeast α-mating-factor gene MFα1 varies considerably between closely related isolates of both Saccharomyces cerevisiae and its sister species Saccharomyces paradoxus. Variation in repeat number has important phenotypic consequences: Increasing repeat number caused higher pheromone production and greater competitive mating success. However, the magnitude of the improvement decreased with increasing repeat number such that repeat amplification beyond that observed in natural isolates failed to generate more pheromone, and could actually reduce sexual fitness. We investigate multiple explanations for this pattern of diminishing returns and find that our results are most consistent with a translational trade-off: Increasing the number of encoded repeats results in more mature pheromone per translation event, but also generates longer transcripts thereby reducing the rate of translation—a phenomenon known as length-dependent translation. Length-dependent translation may be a powerful constraint on the evolution of genes encoding repetitive or modular proteins, with important physiological and behavioral consequences across eukaryotes.

Errors in meiosis can be important postzygotic barriers between different species. In Saccharomyces hybrids, chromosomal missegregation during meiosis I produces gametes with missing or extra chromosomes. Gametes with missing chromosomes are inviable, but we do not understand how extra chromosomes (disomies) influence hybrid gamete inviability. We designed a model predicting rates of missegregation in interspecific hybrid meioses assuming several different mechanisms of disomy tolerance, and compared predictions from the model with observations of sterility in hybrids between Saccharomyces yeast species. Sterility observations were consistent with the hypothesis that chromosomal missegregation causes hybrid sterility, and the model indicated that missegregation probabilities of 13-50% per chromosome can cause observed values of 90-99% hybrid sterility regardless of how cells tolerate disomies. Missing chromosomes in gametes are responsible for most infertility, but disomies may kill as many as 11% of the gametes produced by hybrids between Saccharomyces cerevisiae and Saccharomyces paradoxus. Copyright © 2017 John WileySons, Ltd.

Microbial fitness is easy to measure in the laboratory, but difficult to measure in the field. Laboratory fitness assays make use of controlled conditions and genetically modified organisms, neither of which are available in the field. Among other applications, fitness assays can help researchers detect adaptation to different habitats or locations. We designed a competitive fitness assay to detect adaptation of Saccharomyces paradoxus isolates to the habitat they were isolated from (oak or larch leaf litter). The assay accurately measures relative fitness by tracking genotype frequency changes in the field using digital droplet PCR (DDPCR). We expected locally adapted S. paradoxus strains to increase in frequency over time when growing on the leaf litter type from which they were isolated. The DDPCR assay successfully detected fitness differences among S. paradoxus strains, but did not find a tendency for strains to be adapted to the habitat they were isolated from. Instead, we found that the natural alleles of the hexose transport gene we used to distinguish S. paradoxus strains had significant effects on fitness. The origin of a strain also affected its fitness: strains isolated from oak litter were generally fitter than strains from larch litter. Our results suggest that dispersal limitation and genetic drift shape S. paradoxus populations in the forest more than local selection does, although further research is needed to confirm this. Tracking genotype frequency changes using DDPCR is a practical and accurate microbial fitness assay for natural environments.

The performance of hybrids relative to their parents is an important factor in speciation research. We measured the growth of 46 Saccharomyces yeast F1 interspecific and intraspecific hybrids, relative to the growth of each of their parents, in pairwise competition assays. We found that the growth of a hybrid relative to the average of its parents, a measure of mid‐parent heterosis, correlated with the difference in parental growth relative to their hybrid, a measure of phenotypic divergence, which is consistent with simple complementation of low fitness alleles in one parent by high fitness alleles in the other. Interspecific hybrids showed stronger heterosis than intraspecific hybrids. To manipulate parental phenotypic divergence independently of genotype, we also measured the competitive growth of a single interspecific hybrid relative to its parents in 12 different environments. In these assays, we not only identified a strong relationship between parental phenotypic divergence and mid‐parent heterosis as before, but, more tentatively, a weak relationship between phenotypic divergence and best‐parent heterosis, suggesting that complementation of deleterious mutations was not the sole cause of interspecific heterosis. Our results show that mating between different species can be beneficial, and demonstrate that competition assays between parents and offspring are a useful way to study the evolutionary consequences of hybridization.

In unicellular organisms like yeast, mating with the right partner is critical to future fitness because each individual can only mate once. Because cell size is important for viability, mating with a partner of the right size could be a significant advantage. To investigate this idea, we manipulated the size of unmated yeast cells and showed that their viability depended on environmental conditions; large cells do better on rich medium and small cells do better on poor medium. We also found that the fitness of offspring is determined by the size of their parents. Finally, we demonstrated that when a focal cell of one mating type was placed with a large and a small cell of the opposite mating type, it was more likely to mate with the cell that was closer to the optimum size for growth in a given environment. This pattern was not generated by differences in passive mating efficiency of large and small cells across environments but by competitive mating behavior, mate preference, or both. We conclude that the most likely mechanism underlying this interesting behavior is that yeast cells compete for mates by producing pheromone signals advertising their viability, and cells with the opportunity to choose prefer to mate with stronger signalers because such matings produce more viable offspring.

Models of mRNA translation usually presume that transcripts are linear; upon reaching the end of a transcript each terminating ribosome returns to the cytoplasmic pool before initiating anew on a different transcript. A consequence of linear models is that faster translation of a given mRNA is unlikely to generate more of the encoded protein, particularly at low ribosome availability. Recent evidence indicates that eukaryotic mRNAs are circularized, potentially allowing terminating ribosomes to preferentially reinitiate on the same transcript. Here we model the effect of ribosome reinitiation on translation and show that, at high levels of reinitiation, protein synthesis rates are dominated by the time required to translate a given transcript. Our model provides a simple mechanistic explanation for many previously enigmatic features of eukaryotic translation, including the negative correlation of both ribosome densities and protein abundance on transcript length, the importance of codon usage in determining protein synthesis rates, and the negative correlation between transcript length and both codon adaptation and 5' mRNA folding energies. In contrast to linear models where translation is largely limited by initiation rates, our model reveals that all three stages of translation - initiation, elongation, and termination/reinitiation - determine protein synthesis rates even at low ribosome availability.

Spores from wild yeast isolates often show great variation in the size of colonies they produce, for largely unknown reasons. Here we measure the colonies produced from single spores from six different wild Saccharomyces paradoxus strains. We found remarkable variation in spore colony sizes, even among spores that were genetically identical. Different strains had different amounts of variation in spore colony sizes, and variation was not affected by the number of preceding meioses, or by spore maturation time. We used time-lapse photography to show that wild strains also have high variation in spore germination timing, providing a likely mechanism for the variation in spore colony sizes. When some spores from a laboratory strain make small colonies, or no colonies, it usually indicates a genetic or meiotic fault. Here, we demonstrate that in wild strains spore colony size variation is normal. We discuss and assess potential adaptive and non-adaptive explanations for this variation.

Background Reported prevalence of emotional distress in cancer patients varies widely across studies. The present study determined prevalence of anxiety and depression (separated for presence of symptoms versus clinical levels) in a large, representative sample of cancer patients after diagnosis. Method During the years 2004–2009, 10,153 consecutive patients were routinely screened with the Psychosocial Screen for Cancer questionnaire at two major cancer centers. Results Patients' mean age was 59 years and 45% were men. Across cancer types, 19.0% of patients showed clinical levels of anxiety and another 22.6% had subclinical symptoms. Further, 12.9% of patients reported clinical symptoms of depression and an additional 16.5% described subclinical symptoms. Analyses by cancer type revealed significant differences such that patients with lung, gynecological, or hematological cancer reported the highest levels of distress at the time point of cancer diagnosis. As expected, women showed higher rates of anxiety and depression, and for some cancer types the prevalence was two to three times higher than that seen for men. In some cancer types emotional distress was inversely related to age. Patients younger than 50 and women across all cancer types revealed either subclinical or clinical levels of anxiety in over 50% of cases. Limitations Findings describe levels of emotional distress after diagnosis but cannot inform about trajectories of anxiety and depression over time. Conclusion Given that levels of anxiety and depression varied widely by cancer type, gender, and age, these results inform which cancer patients are most likely in need of psychosocial support.

Saccharomyces cerevisiae yeast cells court each other by producing an attractive sex pheromone specific to their mating type. Cells detect the sex pheromone from potential mates using a well-defined intracellular signalling cascade that has become a model for studying signal transduction. In contrast, the factors contributing to the production of pheromone itself are poorly characterized, despite the widespread use of the S. cerevisiae α-pheromone secretion pathway in industrial fungal protein expression systems. Progress in understanding pheromone secretion has been hindered by a lack of a precise and quantitative pheromone production assay. Here, we present an ELISA-based method for the quantification of α-pheromone secretion. In the absence of pheromone from the opposite mating type, we found that each cell secretes over 550 mature α-pheromone peptides per second; 90% of this total was produced from MF α1. The addition of a-pheromone more than doubled total α-pheromone secretion. This technique offers several improvements on current methods for measuring α-pheromone production and will allow detailed investigation of the factors regulating pheromone production in yeast.

Meiosis in Saccharomyces yeast produces four haploid gametes that usually fuse with each other, an extreme form of self-fertilization among the products of a single meiosis known as automixis. The gametes signal to each other with sex pheromone. Better-quality gametes produce stronger signals and are preferred as mates. We suggest that the function of this signalling system is to enable mate choice among the four gametes from a single meiosis and so to promote the clearance of deleterious mutations. To support this claim, we construct a mathematical model that shows that signalling during automixis (i) improves the long-term fitness of a yeast colony and (ii) lowers its mutational load. We also show that the benefit to signalling is greater with larger numbers of segregating mutations.

The handicap principle holds that costly sexual signals can reliably indicate mate quality. Only individuals of high quality can afford a strong signal—the cost of signaling is relatively lower for high-quality signalers than for low-quality signalers. This critical property is difficult to test experimentally because the benefit of signaling on mating success, and cost of signaling on other components of fitness, cannot easily be separated in obligate sexual organisms. We therefore studied the facultatively sexual yeast Saccharomyces cerevisiae, which produces pheromones to attract potential mates. To precisely measure the cost of signaling, the signal was reduced or removed by deleting one or both copies of the pheromone-encoding genes and measuring asexual growth rate in competition with a wild-type signaler. We manipulated signaler quality either by changing the quality of the assay environment or by changing the number of deleterious mutations carried. For both types of treatment, we found that the cost of signaling decreased as the quality of the signaler increased, demonstrating that the yeast pheromone signal has the key property required for selection under the handicap principle. We found that cells of high genetic quality produce stronger signals than low-quality cells, verifying that the signal is indeed honest.

Yeast technology began when mankind learned how to brew a pleasant drink, and it has since developed unprecedented scientific power. This power is now being applied to ecology and evolution, with several impressive initial successes. This is not merely a good application of yeast technology to a new field, it is also a way to increase the power of that technology further. We cannot properly interpret the enormous data being produced from model laboratory yeast without knowledge about the environment that yeast evolved in. Determining the natural history of yeast is a daunting challenge but metagenomics, the analysis of environmental DNA without laboratory culturing, offers the possibility of unbiased sampling of the microbial communities in which yeast live. With sufficient knowledge of the abundance of yeast in space and time, combined with further population genetic and experimental methods, we can perhaps start to see the world from a yeast's point of view.

The fundamental principle underlying sexual selection theory is that an allele conferring an advantage in the competition for mates will spread through a population. Remarkably, this has never been demonstrated empirically. We have developed an experimental system using yeast for testing genetic models of sexual selection. Yeast signal to potential partners by producing an attractive pheromone; stronger signallers are preferred as mates. We tested the effect of high and low levels of sexual selection on the evolution of a gene determining the strength of this signal. Under high sexual selection, an allele encoding a stronger signal was able to invade a population of weak signallers, and we observed a corresponding increase in the amount of pheromone produced. By contrast, the strong signalling allele failed to invade under low sexual selection. Our results demonstrate, for the first time, the spread of a sexually selected allele through a population, confirming the central assumption of sexual selection theory. Our yeast system is a powerful tool for investigating the genetics of sexual selection.

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.

Although speciation is one of the most interesting processes in evolution, the underlying causes of reproductive isolation are only partially understood in a few species. This review summarizes the results of many experiments on the reproductive isolation between yeast species of the Saccharomyces sensu stricto group. Hybrids between these species form quite readily in the laboratory, but, if given a choice of species to mate with, some are able to avoid hybridization. F1 hybrids are viable but sterile: the gametes they produce are inviable. For one pair of species, hybrid sterility is probably caused by chromosomal rearrangements, but for all the other species, the major cause of hybrid sterility is antirecombination-the inability of diverged chromosomes to form crossovers during F1 hybrid meiosis. Surprisingly, incompatibility between the genes expressed from different species' genomes is not a major cause of F1 hybrid sterility, although it may contribute to reproductive isolation at other stages of the yeast life cycle.

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.

High-throughput population genomics reveals how the evolution of chromosome arrangement and sequence divergence followed by secondary contact upon glacier retreat initiates homoploid hybrid speciation in natural populations of the budding yeast Saccharomyces paradoxus.

SummaryWhen two tribes of Myxococcus bacteria attack each other, the most numerous usually wins. Established colonies can therefore resist invaders by outnumbering them. This shows how positive frequency dependence can maintain diversity across spatially structured environments.

Different species are usually thought to have specific adaptations, which allow them to occupy different ecological niches. But recent neutral ecology theory suggests that species diversity can simply be the result of random sampling, due to finite population sizes and limited dispersal. Neutral models predict that species are not necessarily adapted to specific niches, but are functionally equivalent across a range of habitats. Here, we evaluate the ecology of Saccharomyces cerevisiae, one of the most important microbial species in human history. The artificial collection, concentration and fermentation of large volumes of fruit for alcohol production produce an environment in which S. cerevisiae thrives, and therefore it is assumed that fruit is the ecological niche that S. cerevisiae inhabits and has adapted to. We find very little direct evidence that S. cerevisiae is adapted to fruit, or indeed to any other specific niche. We propose instead a neutral nomad model for S. cerevisiae, which we believe should be used as the starting hypothesis in attempting to unravel the ecology of this important microbe., It is assumed that Saccharomyces cerevisiae is adapted to inhabit fruits; however, we find very little evidence for adaptation to any niche. Instead, we propose a neutral nomad model for S. cerevisiae., Graphical Abstract Figure. It is assumed that Saccharomyces cerevisiae is adapted to inhabit fruits; however, we find very little evidence for adaptation to any niche. Instead, we propose a neutral nomad model for S. cerevisiae.

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.

Complex life has arisen through a series of ‘major transitions’ in which collectives of formerly autonomous individuals evolve into a single, integrated organism. A key step in this process is the origin of higher-level evolvability, but little is known about how higher-level entities originate and gain the capacity to evolve as an individual. Here we report a single mutation that not only creates a new level of biological organization, but also potentiates higher-level evolvability. Disrupting the transcription factor ACE2 in Saccharomyces cerevisiae prevents mother–daughter cell separation, generating multicellular ‘snowflake’ yeast. Snowflake yeast develop through deterministic rules that produce geometrically defined clusters that preclude genetic conflict and display a high broad-sense heritability for multicellular traits; as a result they are preadapted to multicellular adaptation. This work demonstrates that simple microevolutionary changes can have profound macroevolutionary consequences, and suggests that the formation of clonally developing clusters may often be the first step to multicellularity., The first steps in the transition to multicellularity remain poorly understood. Here, the authors demonstrate that disrupting a single gene in yeast results in multicellular clusters that develop clonally and possess a high degree of multicellular heritability, predisposing them to multicellular adaptation.

Homing endonuclease genes (HEGs) in eukaryotes are optional genes that have no obvious effect on host phenotype except for causing chromosomes not containing a copy of the gene to be cut, thus causing them to be inherited at a greater than Mendelian rate via gene conversion. These genes are therefore expected to increase in frequency in outcrossed populations, but not in obligately selfed populations. In order to test this idea, we compared the dynamics of the VDE HEG in six replicate outcrossed and inbred populations of yeast (Saccharomyces cerevisiae). VDE increased in frequency from 0.21 to 0.55 in four outcrossed generations, but showed no change in frequency in the inbred populations. The absence of change in the inbred populations indicates that any effect of VDE on mitotic replication rates is less than 1%. The data from the outcrossed populations best fit a model in which 82% of individuals are derived from outcrossing and VDE is inherited by 74% of the meiotic products from heterozygotes (as compared with 50% for Mendelian genes). These results empirically demonstrate how a host mating system plays a key role in determining the population dynamics of a selfish gene.

Yeast is a superb laboratory model organism, but little is known about its natural lifestyle. Recent studies of wild yeast are beginning to reveal details of Saccharomyces population structure and evolution that challenge assumptions about speciation and dispersal in microbes.

Genetic diversity can be maintained in a heterogeneous environment if different alleles are favoured at different sites [1]. Under these circumstances, organisms that remain local are selected to inbreed in order to conserve locally adapted combinations of alleles [2], but those individuals that disperse should outbreed in order to increase the genetic variance among their progeny [3] and to make it more likely that some inherit combinations of alleles highly adapted to their new site. Here we report experimental results from the budding yeast Saccharomyces cerevisiae that fit with this theoretical prediction.

Models of sexual selection predict that females use ornament size to evaluate male condition. It has also been suggested that ornament asymmetry provides females with accurate information about condition. To test these ideas we experimentally manipulated condition in the stalk-eyed fly, Cyrtodiopsis dalmanni, by varying the amount of food available to developing larvae. Males of this species have greatly exaggerated eyestalk length and females prefer to mate with males with wider eyespans. Our experiments show that male ornaments (eyestalks) display a disproportionate sensitivity to condition compared with the homologous character in females, and to non-sexual traits (wing dimensions). In contrast, in neither sex did asymmetry reflect condition either in sexual ornaments or in non-sexual traits. We conclude that ornament size is likely to play a far greater role in sexual selection as an indicator of individual condition than does asymmetry.

Most explanations for the evolutionary maintenance of sex depend on the assumption that sex produces variation by recombining parental haplotypes in the offspring. Therefore, meiosis is expected to be useful only in heterozygotes. We tested this assumption by competing sexual strains of yeast against constitutive asexuals in a hot (37 degrees C) culture for 500 generations, in either heterozygous or homozygous genetic backgrounds. We found that there was an initial cost of sex for all the sexual strains, which was indicated by a sharp increase in the proportion of asexuals after the induction of sex. The cost was larger in the heterozygotes than in the homozygotes, probably because of recombinational load. However, in two of the three heterozygote backgrounds, after the initial success of the asexuals, the remaining sexuals eventually drove them out of the population. These two heterozygotes also suffered the largest initial cost of sex. In the other heterozygote and in the three homozygote backgrounds it appeared to be a matter of chance whether sexuals or asexuals won. The average relative fitness increased in all the strains, but the increase was largest in the two strains that showed both the clearest advantage and the largest cost of sex. We conclude that these results are consistent with the traditional view that sex has a short-term cost but a long-term benefit.

Lay Summary Yeast cells that are too big or too small are more likely to remain virgins. Big yeast cells are fitter than small cells when food is plentiful, but smaller cells are fitter when food is scarce. When there is a choice of different size potential mates, the best size partner for the conditions is more likely to be chosen for sex, ensuring that the resulting offspring are of a fit size., In unicellular organisms like yeast, mating with the right partner is critical to future fitness because each individual can only mate once. Because cell size is important for viability, mating with a partner of the right size could be a significant advantage. To investigate this idea, we manipulated the size of unmated yeast cells and showed that their viability depended on environmental conditions; large cells do better on rich medium and small cells do better on poor medium. We also found that the fitness of offspring is determined by the size of their parents. Finally, we demonstrated that when a focal cell of one mating type was placed with a large and a small cell of the opposite mating type, it was more likely to mate with the cell that was closer to the optimum size for growth in a given environment. This pattern was not generated by differences in passive mating efficiency of large and small cells across environments but by competitive mating behavior, mate preference, or both. We conclude that the most likely mechanism underlying this interesting behavior is that yeast cells compete for mates by producing pheromone signals advertising their viability, and cells with the opportunity to choose prefer to mate with stronger signalers because such matings produce more viable offspring.

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.

Whole-genome duplication has shaped the genomes of extant lineages ranging from unicellular fungi to vertebrates, and its association with several species-rich taxa has fueled interest in its potential as a catalyst for speciation. One well-established model for the evolution of reproductive isolation involves the reciprocal loss of redundant genes at different loci in allopatric populations. Whole-genome duplication simultaneously doubles the entire gene content of an organism, resulting in massive levels of genetic redundancy and potential for reciprocal gene loss that may produce postzygotic reproductive isolation. Following whole-genome duplication, different populations can potentially change or lose gene function at different duplicate loci. If such populations come back into contact any F1 hybrids that are formed may suffer reduced fertility as some of the gametes they produce may not carry a full complement of functional genes. This reduction in hybrid fertility will be directly proportional to the number of divergently resolved loci between the populations. In this work, we demonstrate that initially identical populations of allotetraploid yeast subjected to mutagenesis rapidly evolve postzygotic reproductive isolation, consistent with the divergent loss of function of redundant gene copies.

Baker's yeast, Saccharomyces cerevisiae, is not only an extensively used model system in genetics and molecular biology, it is an upcoming model for research in ecology and evolution. The available body of knowledge and molecular techniques make yeast ideal for work in areas such as evolutionary and ecological genomics, population genetics, microbial biogeography, community ecology and speciation. As long as ecological information remains scarce for this species, the vast amount of data that is being generated using S. cerevisiae as a model system will remain difficult to interpret in an evolutionary context. Here we review the current knowledge of the evolution and ecology of S. cerevisiae and closely related species in the Saccharomyces sensu stricto group, and suggest future research directions.

Diploid hybrids of Saccharomyces cerevisiae and its closest relative, Saccharomyces paradoxus, are viable, but the sexual gametes they produce are not. One of several possible causes of this gamete inviability is incompatibility between genes from different species—such incompatible genes are usually called “speciation genes.” In diploid F1 hybrids, which contain a complete haploid genome from each species, the presence of compatible alleles can mask the effects of (recessive) incompatible speciation genes. But in the haploid gametes produced by F1 hybrids, recessive speciation genes may be exposed, killing the gametes and thus preventing F1 hybrids from reproducing sexually. Here I present the results of an experiment to detect incompatibilities that kill hybrid gametes. I transferred nine of the 16 S. paradoxus chromosomes individually into S. cerevisiae gametes and tested the ability of each to replace its S. cerevisiae homeolog. All nine chromosomes were compatible, producing nine viable haploid strains, each with 15 S. cerevisiae chromosomes and one S. paradoxus chromosome. Thus, none of these chromosomes contain speciation genes that were capable of killing the hybrid gametes that received them. This is a surprising result that suggests that such speciation genes do not play a major role in yeast speciation., Author Summary A species is usually defined as such because it cannot exchange its genes with other species. Closely related species may attempt to breed but be unsuccessful. A common example of this occurs when a donkey mates with a horse. The offspring of this mating is a hybrid called a mule. Mules are sterile and cannot reproduce, so donkeys and horses are maintained as distinct species—they cannot exchange genes. Understanding what makes hybrids sterile could tell us how new species originate. Instead of mules, this study examines yeast hybrids that are sterile because the sex cells (the yeast equivalent of sperms or eggs) they produce are dead. One possible reason for this is that the genes from the different species fail to work together in the sex cells, killing them. To test this idea, I replaced individual chromosomes in one species' sex cells with chromosomes from another species. Surprisingly, this did not kill the gametes, showing that the genes from one species can work fine with the genes of another. Not all the genes could be tested in this way, but nevertheless it seems likely that the death of sex cells produced by yeast hybrids is caused by something other than failure of the genes from different species to work together.

The SUC multigene family of the single-celled yeast Saccharomyces cerevisiae is polymorphic, with genes varying both in number and activity. All of the genes encode invertase, an enzyme that is secreted to digest sucrose outside of the cell. This communal endeavour creates the potential for individual cells to defect (cheat) by stealing the sugar digested by their neighbours without contributing the enzyme themselves. We measured the fitness of a defector, with a deleted suc2 gene, relative to an otherwise isogenic cooperator, with a functional SUC2 gene. We manipulated the level of social interaction within the community by varying the population density and found that the defector is less fit than the cooperator at low levels of sociality but more fit in dense communities. We propose that selection for antisocial cheating causes SUC polymorphism in nature. The infamous Prisoner's Dilemma game shows that social behaviour is generally unstable, and the success of both cooperation and defection can vary continuously in time and space. The variation in SUC genes reflects constant adaptation to an ever-changing biotic environment that is a consequence of the instability of cooperation. It is interesting that social interactions can have a direct effect on molecular evolution, even in an organism as simple as yeast.