Fermentative yeasts play important roles in both ecological and industrial processes, but their distribution and abundance in natural environments are not well understood. We investigated the diversity of yeasts at the northern range limit of their oak tree hosts (Quercus spp.) in Sweden, and identified climatic and ecological conditions governing their distribution. Yeasts were isolated from bark samples from 28 forests and identified to the species level using DNA metabarcoding. Most communities were dominated by species in the Saccharomycetaceae family, especially by species of Saccharomyces, Kluyveromyces and Pichia. Each genus showed a distinct latitudinal and longitudinal distribution, and both temperature and precipitation metrics predicted significant variation in their abundance. Consistent with this, laboratory assays revealed significant effects of temperature on the growth of strains collected from different longitudes and latitudes. We found that older trees harbour more diverse and more balanced fermentative yeast communities with more evenly distributed species abundances. Communities across trees were more similar when sharing a common dominant species. This work provides a baseline for future studies on the impact of climate change on the fermentative yeast biodiversity of temperate forests in northern latitudes and contributes to a growing collection of wild isolates for potential biotechnological applications.

NOD-like receptors (NLRs) are intracellular immune receptors that detect pathogen-associated cues and trigger defence mechanisms, including regulated cell death. In filamentous fungi, some NLRs mediate heterokaryon incompatibility, a self-/non-self-recognition process that prevents the vegetative fusion of genetically distinct individuals, reducing the risk of parasitism. The het-d and het-e NLRs in Podospora anserina are highly polymorphic incompatibility genes (het genes) whose products recognize different allelic variants of the HET-C protein via a sensor domain composed of WD40 repeats. These repeats display unusually high sequence identity maintained by concerted evolution. However, some sites within individual repeats are hypervariable and under diversifying selection. Despite extensive genetic studies, inconsistencies in the reported WD40 domain sequence have hindered functional and evolutionary analyses. Here, we confirm that the WD40 domain can be accurately reconstructed from long-read sequencing (Oxford Nanopore and PacBio) data, but not from Illumina-based assemblies. Functional alleles are usually formed by 11 highly conserved repeats, with different repeat combinations underlying the same phenotypic het-d and het-e incompatibility reactions. AlphaFold 3 structure models suggest that their WD40 domain folds into two 7-blade β-propellers composed of the highly conserved repeats, as well as three cryptic divergent repeats at the C-terminus. We additionally show that one particular het-e allele does not have an incompatibility reaction with common het-c alleles, despite being 11-repeats long. Finally, we present evidence that the recognition phenotypes of het-e and het-d arose through convergent evolution. Our findings provide a robust foundation for future research into the molecular mechanisms and evolutionary dynamics of het NLRs, while also highlighting both the fragility and the flexibility of β-propellers as immune sensor domains.

Climate warming is threatening biodiversity by increasing temperatures beyond the optima of many ectotherms. Owing to the inherent non-linear relationship between temperature and the rate of cellular processes, such shifts towards hot temperature are predicted to impose stronger selection compared with corresponding shifts towards cold temperature. This suggests that when adaptation to warming occurs, it should be relatively rapid and predictable. Here we tested this hypothesis from the level of single-nucleotide polymorphisms to life-history traits in the beetle Callosobruchus maculatus. We conducted an evolve-and-resequence experiment on three genetic backgrounds of the beetle reared at hot or cold temperature. Indeed, we find that phenotypic evolution was faster and more repeatable at hot temperature. However, at the genomic level, adaptation to heat was less repeatable when compared across genetic backgrounds. As a result, genomic predictions of phenotypic adaptation in populations exposed to hot temperature were accurate within, but not between, backgrounds. These results seem best explained by genetic redundancy and an increased importance of epistasis during adaptation to heat, and imply that the same mechanisms that exert strong selection and increase repeatability of phenotypic evolution at hot temperature reduce repeatability at the genomic level. Thus, predictions of adaptation in key phenotypes from genomic data may become increasingly difficult as climates warm.

Populations evolving independently in divergent environments accumulate genetic differences and potentially evolve reproductive isolation as a by-product of divergence. The speed and mechanisms underlying this process are difficult to investigate because we rarely get the opportunity to witness them in natural settings, and histories of selection and gene flow between populations are often unknown. Here, we experimentally evolved yeast for 1000 generations of evolution in both divergent and parallel environments. At regular time points during experimental evolution, we made crosses between parallel- and divergent-evolving populations to measure postzygotic reproductive isolation (gamete viability). We used whole genome population sequencing to determine the mutational load, the number and types of structural variation, and other genomic features of the parent, F1 and F2 intraspecific hybrids. We found evidence for large-scale phenotypic and genome-wide differentiation in response to divergent laboratory selection. Divergent-selected populations produced hybrids with reduced gamete viability—a classic signature of postzygotic reproductive isolation in the form of hybrid breakdown. Parallel-selected populations, on the other hand, remained more reproductively compatible (with exceptions). We found that F2 hybrid genomes contained vast genomic instability, that is, new structural variants (especially insertions, deletions and interchromosomal translocations) that were not observed in parent and F1 genomes, which is likely a result of chromosome missegregation and recombination errors in hybrid meiosis. Our results provide phenotypic and genomic evidence that partial reproductive isolation evolved due to adaptation to divergent environments, consistent with predictions of ecological speciation theory.

The maintenance of biodiversity crucially depends on the evolutionary potential of populations to adapt to environmental change. Accelerating climate change and extreme temperature events urge us to better understand and forecast evolutionary responses. Here, we harnessed the power of experimental evolution with the microbial model system yeast (Saccharomyces spp.) to measure the evolutionary potential of populations to adapt to future warming, in real-time and across the entire phylogenetic diversity of the genus. We tracked the evolution of thermal performance curves (TPCs) in populations of eight genetically and ecologically diverse species under gradually increasing temperature conditions, from 25 to 40 °C, for up to 600 generations. We found that evolving toward higher critical thermal limits generally came at a cost, causing a decrease in both thermal tolerance and maximum growth performance. The evolution of TPCs varied significantly between species with strong genotype-by-environment interactions, revealing two main trajectories: i) Warm-tolerant species showed an increase in both optimum growth temperature and thermal tolerance, consistent with the “hotter is wider” hypothesis. ii) Cold-tolerant species on the other hand evolved larger thermal breadth and higher thermal limits, but suffered from reduced maximum performance overall, consistent with the generalist or “a jack of all temperatures is a master of none” hypothesis. In addition, cold-tolerant species never reached the warm-tolerant species’ upper thermal limits. Our results show that adaptive strategies to increasing temperatures are complex, highlighting the need to consider both within and between species diversity when predicting and managing the impacts of climate change on populations.

Until recently, our understanding of the genetics of speciation was limited to a narrow group of model species with a specific set of characteristics that made genetic analysis feasible. Rapidly advancing genomic technologies are eliminating many of the distinctions between laboratory and natural systems. In light of these genomic developments, we review the history of speciation genetics, advances that have been gleaned from model and non-model organisms, the current state of the field, and prospects for broadening the diversity of taxa included in future studies. Responses to a survey of speciation scientists across the world reveal the ongoing division between the types of questions that are addressed in model and non-model organisms. To bridge this gap, we suggest integrating genetic studies from model systems that can be reared in the laboratory or greenhouse with genomic studies in related non-models where extensive ecological knowledge exists.

Hybrids between species exhibit plastic genomic architectures that could foster or slow down their adaptation. When challenged to evolve in an environment containing a UV mimetic drug, yeast hybrids have reduced adaptation rates compared to parents. We find that hybrids and their parents converge onto similar molecular mechanisms of adaptation by mutations in pleiotropic transcription factors, but at a different pace. After 100 generations, mutations in these genes tend to be homozygous in the parents but heterozygous in the hybrids. We hypothesize that a lower rate of loss of heterozygosity (LOH) in hybrids could limit fitness gain. Using genome editing, we first demonstrate that mutations display incomplete dominance, requiring homozygosity to show full impact and to entirely circumvent Haldane’s sieve, which favors the fixation of dominant mutations. Second, tracking mutations in earlier generations confirmed a different rate of LOH in hybrids. Together, these findings show that Haldane’s sieve slows down adaptation in hybrids, revealing an intrinsic constraint of hybrid genomic architecture that can limit the role of hybridization in adaptive evolution.

Ecologically mediated selection against hybrids, caused by hybrid phenotypes fitting poor-ly into available niches, is typically viewed as distinct from selection caused by epistatic Dobzhansky–Muller hybrid incompatibilities. Here, we show how selection against trans-gressive phenotypes in hybrids manifests as incompatibility. After outlining our logic, we summarize current approaches for studying ecology-based selection on hybrids. We then quantitatively review QTL-mapping studies and find traits differing between parent taxa are typically polygenic. Next, we describe how verbal models of selection on hybrids translate to phenotypic and genetic fitness landscapes, highlighting emerging approaches for detecting polygenic incompatibilities. Finally, in a synthesis of published data, we report that trait transgression—and thus possibly extrinsic hybrid incompatibility in hybrids—escalates with the phenotypic divergence between parents. We discuss conceptual implications and conclude that studying the ecological basis of hybrid incompatibility will facilitate new discoveries about mechanisms of speciation.

Lager yeasts are limited to a few strains worldwide, imposing restrictions on flavour and aroma diversity and hindering our understanding of the complex evolutionary mechanisms during yeast domestication. The recent finding of diverse S. eubayanus lineages from Patagonia offers potential for generating new lager yeasts with different flavour profiles. Here, we leverage the natural genetic diversity of S. eubayanus and expand the lager yeast repertoire by including three distinct Patagonian S. eubayanus lineages. We used experimental evolution and selection on desirable traits to enhance the fermentation profiles of novel S. cerevisiae x S. eubayanus hybrids. Our analyses reveal an intricate interplay of pre-existing diversity, selection on species-specific mitochondria, de-novo mutations, and gene copy variations in sugar metabolism genes, resulting in high ethanol production and unique aroma profiles. Hybrids with S. eubayanus mitochondria exhibited greater evolutionary potential and superior fitness post-evolution, analogous to commercial lager hybrids. Using genome-wide screens of the parental subgenomes, we identified genetic changes in IRA2, IMA1, and MALX genes that influence maltose metabolism, and increase glycolytic flux and sugar consumption in the evolved hybrids. Functional validation and transcriptome analyses confirmed increased maltose-related gene expression, influencing greater maltotriose consumption in evolved hybrids. This study demonstrates the potential for generating industrially viable lager yeast hybrids from wild Patagonian strains. Our hybridization, evolution, and mitochondrial selection approach produced hybrids with high fermentation capacity and expands lager beer brewing options.

Saccharomyces hybrid yeasts are receiving increasing attention as a powerful model system to understand adaptation to environmental stress and speciation mechanisms, using experimental evolution and omics techniques. We compiled all genomic resources available from public repositories of the eight recognized Saccharomyces species and their interspecific hybrids. We present the newest numbers on genomes sequenced, assemblies, annotations, and sequencing runs, and an updated species phylogeny using orthogroup inference. While genomic resources are highly skewed towards Saccharomyces cerevisiae, there is a noticeable movement to use wild, recently discovered yeast species in recent years. To illustrate the degree and potential causes of reproductive isolation, we reanalyzed published data on hybrid spore viabilities across the entire genus and tested for the role of genetic, geographic, and ecological divergence within and between species (28 cross types and 371 independent crosses). Hybrid viability generally decreased with parental genetic distance likely due to antirecombination and negative epistasis, but notable exceptions emphasize the importance of strain-specific structural variation and ploidy differences. Surprisingly, the viability of crosses within species varied widely, from near reproductive isolation to near-perfect viability. Geographic and ecological origins of the parents predicted cross viability to an extent, but with certain caveats. Finally, we highlight publication trends in the field and point out areas of special interest, where hybrid yeasts are particularly promising for innovation through research and development, and experimental evolution and fermentation.