Dissecting an ancient stress resistance trait syndrome in the compost yeast .

In the search to understand how evolution builds new traits, ancient events are often the hardest to dissect. Species-unique traits pose a particular challenge for geneticists-cases in which a character arose long ago and, in the modern day, is conserved within a species, distinguishing it from reproductively isolated relatives. In this work, we have developed the budding yeast genus as a model for mechanistic dissection of trait variation across species boundaries. Phenotypic profiling revealed robust heat and chemical-stress tolerance phenotypes that distinguished the compost yeast from the rest of the clade. We used culture-based, transcriptomic, and genetic approaches to characterize the metabolic requirements of the trait syndrome. We then generated a population-genomic resource for and harnessed it in molecular-evolution analyses, which found hundreds of housekeeping genes with evidence for adaptive protein variation unique to this species. Our data support a model in which, in the distant past, underwent a vastly complex remodeling of its proteome to achieve stress resistance. Such a polygenic architecture, involving nucleotide-level allelic variation on a massive scale, is consistent with theoretical models of the mechanisms of long-term adaptation, and suggests principles of broad relevance for interspecies trait genetics.