Joint effects of genes underlying a temperature specialization tradeoff in yeast

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 other’s 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.