Joint effects of genes underlying a temperature specialization tradeoff in yeast

Abstract

A central goal of evolutionary genetics is to understand, at the molecular level, how organisms adapt to their environments. For a given trait, the answer often involves the acquisition of variants at unlinked sites across the genome. Genomic methods have achieved landmark successes in pinpointing adaptive loci. To figure out how a suite of adaptive alleles work together, and to what extent they can reconstitute the phenotype of interest, requires their transfer into an exogenous background. We studied the joint effect of adaptive, gain-of-function thermotolerance alleles at eight unlinked genes from Saccharomyces cerevisiae, when introduced into a thermosensitive sister species, S. paradoxus. Although the loci damped each others beneficial impact (that is, they were subject to negative epistasis), most boosted high-temperature growth alone and in combination, and none was deleterious. The complete set of eight genes was sufficient to confer [~]15% of the S. cerevisiae phenotype in the S. paradoxus background. The same loci also contributed to a heretofore unknown advantage in cold growth by S. paradoxus. Together, our data establish temperature resistance in yeasts as a model case of a genetically complex evolutionary tradeoff, which can be partly reconstituted from the sequential assembly of unlinked underlying loci. Author summaryOrganisms adapt to threats in the environment by acquiring DNA sequence variants that tweak traits to improve fitness. Experimental studies of this process have proven to be a particular challenge when they involve manipulation of a suite of genes, all on different chromosomes. We set out to understand how so many loci could work together to confer a trait. We used as a model system eight genes that govern the ability of the unicellular yeast Saccharomyces cerevisiae to grow at high temperature. We introduced these variant loci stepwise into a non-thermotolerant sister species, and found that the more S. cerevisiae alleles we added, the better the phenotype. We saw no evidence for toxic interactions between the genes as they were combined. We also used the eight-fold transgenic to dissect the biological mechanism of thermotolerance. And we discovered a tradeoff: the same alleles that boosted growth at high temperature eroded the organisms ability to deal with cold conditions. These results serve as a case study of modular construction of a trait from nature, by assembling the genes together in one genome.