Temperature preference biases parental genome retention during hybrid evolution

Abstract

9Interspecific hybridization can introduce genetic variation that aids in adaptation to new or 10 changing environments. Here we investigate how the environment, and more specifically 11 temperature, interacts with hybrid genomes to alter parental genome representation over time. 12 We evolved Saccharomyces cerevisiae x Saccharomyces uvarum hybrids in nutrient-limited 13 continuous culture at 15°C for 200 generations. In comparison to previous evolution experiments 14 at 30°C, we identified a number of temperature specific responses, including the loss of the S. 15 cerevisiae allele in favor of the cryotolerant S. uvarum allele for several portions of the hybrid 16 genome. In particular, we discovered a genotype by environment interaction in the form of a 17 reciprocal loss of heterozygosity event on chromosome XIII. Which species haplotype is lost or 18 maintained is dependent on the parental species temperature preference and the temperature at 19 which the hybrid was evolved. We show that a large contribution to this directionality is due to 20 temperature sensitivity at a single locus, the high affinity phosphate transporter PHO84. This 21 work helps shape our understanding of what forces impact genome evolution after hybridization, 22 and how environmental conditions may favor or disfavor hybrids over time. 23 24 uvarum strains show evidence of introgression from several other yeast species, and S. cerevisiae 71x S. uvarum hybrids have been isolated from fermentation environments [55,59]. 72 We previously evolved S. cerevisiae x S. uvarum hybrids in the laboratory in several 73 nutrient-limited environments at the preferred growth temperature of S. cerevisiae [60]. We 74 frequently observed a phenomenon known as loss of heterozygosity (LOH) in these evolved 75 hybrids, in which an allele from one species is lost while the other species' allele is maintained. 76The outcome of such events is the homogenization of the hybrid genome at certain loci, and 77 represents a way in which a hybrid genome may become biased toward one parent's sub-78 genome. This type of mutation can occur due to gene conversion or break induced repair, and as 79 previously noted, has also been observed in organisms including S. pastorianus, pathogenic 80 hybrid yeast, and hybrid plants, but its role in adaptation has been unclear [47,61,62]. We used 81 genetic manipulation and competitive fitness assays to show that a particular set of LOH events 82 was the result of selection on the loss of the S. uvarum allele and amplification of the S. 83 cerevisiae allele at the high affinity phosphate transporter PHO84 in phosphate limited 84 conditions. By empirically demonstrating that LOH can be the product of selection, we 85 illuminated how an underappreciated mutation class can underlie adaptive hybrid phenotypes. 86This prior study illuminated how the environment (differences in nutrient availability) 87 can bias a hybrid genome towards one parent sub-genome. Due to many examples of genotype 88 by temperature interactio...

Laboratory Evolution of a Saccharomyces cerevisiae × S. eubayanus Hybrid Under Simulated Lager-Brewing Conditions

“…Instead, in all cases, genetic material was lost due to internal deletions, or genetic material from one chromosome was replaced by an additional copy of genetic material from another chromosome. This abundant loss of heterozygosity is consistent with the evolutionary history of S. cerevisiae (Magwene et al, 2011) and with previously observed loss of genetic material in hybrids (Sipiczki, 2008; Peris et al, 2017; Smukowski Heil et al, 2017, 2018). Under selective conditions, regions from one subgenome can be preferentially affected by loss of heterozygosity due to the fitness effects of genes they harbor.…”

Epistasis, aneuploidy, and gain-of-function mutations underlie the evolution of resistance to induced microtubule depolymerization

“…The effect depended on the tub2-401 allele, since two copies of the same chromosome impaired growth in the presence of wild type TUB2 ( Figure 5C). Finally, for cells expressing TUB2, we observed that growth at low temperature was improved by the deletion of PHO4 ( Figure S4A), in agreement with a role for phosphate uptake in adaptation to the cold [34,43].…”

Fitness Benefits of Loss of Heterozygosity in SaccharomycesHybrids

“…LOH is prevalent in hybrid genomes across taxa. In our previous work, we observed these events arising quickly in interspecific yeast hybrids during only a few hundred generations of laboratory selection (Smukowski Heil et al 2017;2018b). In this study, we found specific gene deletions within these regions that might contribute to the fitness benefits enjoyed by these evolved strains, and we broadened our analysis to the whole genome to determine how hemizygous deletions behave more generally.…”

“…In order to understand hybrid LOH, in this study we utilized two divergent species: S. cerevisiae and S. uvarum. We previously evolved hybrids and diploids of these species in nutrient-limited chemostat culture (Gresham et al 2008;Sanchez et al 2017a;Smukowski Heil et al 2017;2018b). We created thousands of S. cerevisiae x S. uvarum hybrid yeast strains by mating the S. cerevisiae nonessential deletion collection to WT S. uvarum.…”