Patterns of Genomic Instability in Interspecific Yeast Hybrids With Diverse Ancestries

Abstract

The genomes of hybrids often show substantial deviations from the features of the parent genomes, including genomic instabilities characterized by chromosomal rearrangements, gains, and losses. This plastic genomic architecture generates phenotypic diversity, potentially giving hybrids access to new ecological niches. It is however unclear if there are any generalizable patterns and predictability in the type and prevalence of genomic variation and instability across hybrids with different genetic and ecological backgrounds. Here, we analyzed the genomic architecture of 204 interspecific Saccharomyces yeast hybrids isolated from natural, industrial fermentation, clinical, and laboratory environments. Synchronous mapping to all eight putative parental species showed significant variation in read depth indicating frequent aneuploidy, affecting 44% of all hybrid genomes and particularly smaller chromosomes. Early generation hybrids with largely equal genomic content from both parent species were more likely to contain aneuploidies than introgressed genomes with an older hybridization history, which presumably stabilized the genome. Shared k-mer analysis showed that the degree of genomic diversity and variability varied among hybrids with different parent species. Interestingly, more genetically distant crosses produced more similar hybrid genomes, which may be a result of stronger negative epistasis at larger genomic divergence, putting constraints on hybridization outcomes. Mitochondrial genomes were typically inherited from the species also contributing the majority nuclear genome, but there were clear exceptions to this rule. Together, we find reliable genomic predictors of instability in hybrids, but also report interesting cross- and environment-specific idiosyncrasies. Our results are an important step in understanding the factors shaping divergent hybrid genomes and their role in adaptive evolution.

Macroevolutionary diversity of traits and genomes in the model yeast genus Saccharomyces

“…The role of introgressions during lineage diversification is still under debate, but nuclear introgressions between species have been mainly observed in human-associated environments, including the horizontal gene transfer of few genes [82][83][84] , frequent admixture of domesticated S. cerevisiae strains 13,36,62 , and interspecies hybridization of strains used to produce fermented beverages [85][86][87] . In contrast, cytoplasmic genetic elements have undergone extensive introgression and gene flow even in wild strains of Saccharomyces, as previously seen in animals [88][89][90] .…”

Saccharomyces yeast hybrids on the rise

“…Counts are colored on a lognormalized scale for each category (white-orange-red) [Colour figure can be viewed at wileyonlinelibrary.com] (Figure 2a). Of the 28 two-species combinations, only six combinations have available genomes, and these are dominated by S. cerevisiae  S. eubayanus crosses ($47%), many of which are closely related to each other and very similar in their genomic composition (Bendixsen, Peris, et al, 2021). S. cerevisiae  S. eubayanus hybrids, also known as S. pastorianus, are the most common interspecific hybrids used for brewing.…”

“…Introgression is used as genetic evidence for past hybrid matings followed by backcrossing and other postzygotic processes, causing an imbalance in the relative contributions of the parental genomes. Bendixsen, Peris, et al, (2021) recently identified a relationship between parental contributions and aneuploidy in hybrids using read depth analysis: The larger the difference in parental genomic content in the hybrid genome, the fewer aneuploidies were detected, which is likely a result of increasing genome stabilization after hybridization event.…”

“…Introgression is common in domesticated species (Almeida et al, 2014; Peter et al, 2018) but has also been found in wild populations (Almeida et al, 2017; Liti et al, 2006), affecting both the nuclear and mitochondrial genome (Peris, Arias, et al, 2017). Introgression from S. paradoxus into S. cerevisiae is particularly common with up to hundreds of open reading frames (ORF) identified (Bendixsen, Peris, et al, 2021; Peter et al, 2018). In fact, all S. cerevisiae isolates have been shown to carry at least one S. paradoxus gene, suggesting pervasive gene‐flow between the two species (Peter et al, 2018).…”

“…Hybridization also substantially contributed to generating the diversity of microbial fungal species we see today (Dujon & Louis, 2017; Taylor & Larson, 2019). Our understanding of the evolutionary outcomes of hybridization in the yeast genus Saccharomyces is constantly growing and includes genomic, physiological, and ecological impacts of hybridization (Alsammar & Delneri, 2020; Bendixsen, Peris, et al, 2021; Brice et al, 2021; Gabaldón, 2020; Lancaster et al, 2019; Pérez‐Través et al, 2014; Smukowski Heil et al, 2019).…”