Recombination rate in Drosophila species shapes the impact of selection in the genome and is positively correlated with nucleotide diversity.

Hybridization is often considered maladaptive, but sometimes hybrids can invade new ecological niches and adapt to novel or stressful environments better than their parents. The genomic changes that occur following hybridization that facilitate genome resolution and/or adaptation are not well understood. Here, we examine hybrid genome evolution using experimental evolution of de novo interspecific hybrid yeast Saccharomyces cerevisiae × Saccharomyces uvarum and their parentals. We evolved these strains in nutrient-limited conditions for hundreds of generations and sequenced the resulting cultures identifying numerous point mutations, copy number changes, and loss of heterozygosity (LOH) events, including species-biased amplification of nutrient transporters. We focused on a particularly interesting example, in which we saw repeated LOH at the high-affinity phosphate transporter gene PHO84 in both intra- and interspecific hybrids. Using allele replacement methods, we tested the fitness of different alleles in hybrid and S. cerevisiae strain backgrounds and found that the LOH is indeed the result of selection on one allele over the other in both S. cerevisiae and the hybrids. This is an example where hybrid genome resolution is driven by positive selection on existing heterozygosity and demonstrates that even infrequent outcrossing may have lasting impacts on adaptation.

Yeast flocculation is a community-building cell aggregation trait that is an important mechanism of stress resistance and a useful phenotype for brewers; however, it is also a nuisance in many industrial processes, in clinical settings, and in the laboratory. Chemostat-based evolution experiments are impaired by inadvertent selection for aggregation, which we observe in 35% of populations. These populations provide a testing ground for understanding the breadth of genetic mechanisms Saccharomyces cerevisiae uses to flocculate, and which of those mechanisms provide the biggest adaptive advantages. In this study, we employed experimental evolution as a tool to ask whether one or many routes to flocculation are favored, and to engineer a strain with reduced flocculation potential. Using a combination of whole genome sequencing and bulk segregant analysis, we identified causal mutations in 23 independent clones that had evolved cell aggregation during hundreds of generations of chemostat growth. In 12 of those clones, we identified a transposable element insertion in the promoter region of known flocculation gene FLO1, and, in an additional five clones, we recovered loss-of-function mutations in transcriptional repressor TUP1, which regulates FLO1 and other related genes. Other causal mutations were found in genes that have not been previously connected to flocculation. Evolving a flo1 deletion strain revealed that this single deletion reduces flocculation occurrences to 3%, and demonstrated the efficacy of using experimental evolution as a tool to identify and eliminate the primary adaptive routes for undesirable traits.

Meiotic recombination rate varies across the genome within and between individuals, populations, and species in virtually all taxa studied. In almost every species, this variation takes the form of discrete recombination hotspots, determined in some mammals by a protein called PRDM9. Hotspots and their determinants have a profound effect on the genomic landscape, and share certain features that extend across the tree of life. Drosophila, in contrast, are anomalous in their absence of hotspots, PRDM9, and other species-specific differences in the determination of recombination. To better understand the evolution of meiosis and general patterns of recombination across diverse taxa, we present a truly comprehensive portrait of recombination across time, combining recently published cross-based contemporary recombination estimates from each of two sister species with newly obtained linkage-disequilibrium-based historic estimates of recombination from both of these species. Using Drosophila pseudoobscura and Drosophila miranda as a model system, we compare recombination rate between species at multiple scales, and we suggest that Drosophila replicate the pattern seen in human–chimpanzee in which recombination rate is conserved at broad scales. We also find evidence of a species-wide recombination modifier(s), resulting in both a present and historic genome-wide elevation of recombination rates in D. miranda, and identify broad scale effects on recombination from the presence of an inversion. Finally, we reveal an unprecedented view of the distribution of recombination in D. pseudoobscura, illustrating patterns of linked selection and where recombination is taking place. Overall, by combining these estimation approaches, we highlight key similarities and differences in recombination between Drosophila and other organisms.

The yeast Saccharomyces cerevisiae has been instrumental in the fermentation of foods and beverages for millennia. In addition to fermentations like wine, beer, cider, sake, and bread, S. cerevisiae has been isolated from environments ranging from soil and trees, to human clinical isolates. Each of these environments has unique selection pressures that S. cerevisiae must adapt to. Bread dough, for example, requires S. cerevisiae to efficiently utilize the complex sugar maltose; tolerate osmotic stress due to the semi-solid state of dough, high salt, and high sugar content of some doughs; withstand various processing conditions, including freezing and drying; and produce desirable aromas and flavors. In this review, we explore the history of bread that gave rise to modern commercial baking yeast, and the genetic and genomic changes that accompanied this. We illustrate the genetic and phenotypic variation that has been documented in baking strains and wild strains, and how this variation might be used for baking strain improvement. While we continue to improve our understanding of how baking strains have adapted to bread dough, we conclude by highlighting some of the remaining open questions in the field.

Barbara McClintock first hypothesized that interspecific hybridization could provide a “genomic shock” that leads to the mobilization of transposable elements. This hypothesis is based on the idea that regulation of transposable element movement is potentially disrupted in hybrids. However, the handful of studies testing this hypothesis have yielded mixed results. Here, we set out to identify if hybridization can increase transposition rate and facilitate colonization of transposable elements in Saccharomyces cerevisiae x Saccharomyces uvarum interspecific yeast hybrids. S. cerevisiae have a small number of active long terminal repeat (LTR) retrotransposons (Ty elements), while their distant relative S. uvarum have lost the Ty elements active in S. cerevisiae. While the regulation system of Ty elements is known in S. cerevisiae, it is unclear how Ty elements are regulated in other Saccharomyces species, and what mechanisms contributed to the loss of most classes of Ty elements in S. uvarum. Therefore, we first assessed whether transposable elements could insert in the S. uvarum sub-genome of a S. cerevisiae x S. uvarum hybrid. We induced transposition to occur in these hybrids and developed a sequencing technique to show that Ty elements insert readily and non-randomly in the S. uvarum genome. We then used an in vivo reporter construct to directly measure transposition rate in hybrids, demonstrating that hybridization itself does not alter rate of mobilization. However, we surprisingly show that species-specific mitochondrial inheritance can change transposition rate by an order of magnitude. Overall, our results provide evidence that hybridization can potentially facilitate the introduction of transposable elements across species boundaries and alter transposition via mitochondrial transmission, but that this does not lead to unrestrained proliferation of transposable elements suggested by the genomic shock theory.

Interspecific hybridization can introduce genetic variation that aids in adaptation to new or changing environments. Here, we investigate how hybrid adaptation to temperature and nutrient limitation may alter parental genome representation over time. We evolved Saccharomyces cerevisiae x Saccharomyces uvarum hybrids in nutrient-limited continuous culture at 15°C for 200 generations. In comparison to previous evolution experiments at 30°C, we identified a number of responses only observed in the colder temperature regime, including the loss of the S. cerevisiae allele in favor of the cryotolerant S. uvarum allele for several portions of the hybrid genome. In particular, we discovered a genotype by environment interaction in the form of a loss of heterozygosity event on chromosome XIII; which species’ haplotype is lost or maintained is dependent on the parental species’ temperature preference and the temperature at which the hybrid was evolved. We show that a large contribution to this directionality is due to a temperature dependent fitness benefit at a single locus, the high affinity phosphate transporter gene PHO84. This work helps shape our understanding of what forces impact genome evolution after hybridization, and how environmental conditions may promote or disfavor the persistence of hybrids over time.

Meiotic recombination rate varies across the genome within and between individuals, populations, and species in virtually all taxa studied. In almost every species, this variation takes the form of discrete recombination hotspots, determined in some mammals by a protein called PRDM9. Hotspots and their determinants have a profound effect on the genomic landscape, and share certain features that extend across the tree of life. Drosophila, in contrast, are anomalous in their absence of hotspots, PRDM9, and other speciesspecific differences in the determination of recombination. To better understand the evolution of meiosis and general patterns of recombination across diverse taxa, we present a truly comprehensive portrait of recombination across time, combining recently published cross-based contemporary recombination estimates from each of two sister species with newly obtained linkage-disequilibrium-based historic estimates of recombination from both of these species. Using Drosophila pseudoobscura and Drosophila miranda as a model system, we compare recombination rate between species at multiple scales, and we suggest that Drosophila replicate the pattern seen in human-chimpanzee in which recombination rate is conserved at broad scales. We also find evidence of a species-wide recombination modifier(s), resulting in both a present and historic genome-wide elevation of recombination rates in D. miranda, and identify broad scale effects on recombination from the presence of an inversion. Finally, we reveal an unprecedented view of the distribution of recombination in D. pseudoobscura, illustrating patterns of linked selection and where recombination is taking place. Overall, by combining these estimation approaches, we highlight key similarities and differences in recombination between Drosophila and other organisms.