Abstract

Quantitative genetics aims to map genotype to phenotype, often with the goal of understanding how organisms evolved. However, it remains unclear whether the genetic variants identified are exemplary of evolution. Here we analyzed progeny of two wild Saccharomyces cerevisiae isolates to identify 195 loci underlying complex metabolic traits, resolving 107 to single polymorphisms with diverse molecular mechanisms. More than 20% of causal variants exhibited patterns of emergence inconsistent with neutrality. Moreover, contrary to drift-centric expectation, variation in diverse wild yeast isolates broadly exhibited this property: over 30% of shared natural variants exhibited phylogenetic signatures suggesting that they are not neutral. This pattern is likely attributable to both homoplasy and balancing selection on ancestral polymorphism. Variants that emerged repeatedly were more likely to have done so in isolates from the same ecological niche. Our results underscore the power of super-resolution mapping of ecologically relevant traits in understanding adaptation and evolution.

Highlights

  • Quantitative genetics aims to map genotype to phenotype, often with the goal of understanding how organisms evolved

  • This torrent of data has improved the resolution of quantitative trait locus (QTL) determination, most such associations between genotype and phenotype remain resistant to mapping at the single-gene, let alone single-nucleotide, level without exhaustive experimental follow-up[5,6,7]

  • We identify QTNs for genetically complex and ecologically relevant traits in a cross between two wild parental isolates, focusing on metabolic traits critical for the adaptation of S. cerevisiae strains to their diverse ecological niches[10,11,12]

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Summary

Introduction

Quantitative genetics aims to map genotype to phenotype, often with the goal of understanding how organisms evolved. It remains controversial whether such variants are representative of those that drive evolution in the wild because many of the chemical insults in question are unlikely to be encountered by yeast in their natural environments[9] To address this question, we identify QTNs for genetically complex and ecologically relevant traits in a cross between two wild parental isolates, focusing on metabolic traits critical for the adaptation of S. cerevisiae strains to their diverse ecological niches[10,11,12]. We identify QTNs for genetically complex and ecologically relevant traits in a cross between two wild parental isolates, focusing on metabolic traits critical for the adaptation of S. cerevisiae strains to their diverse ecological niches[10,11,12] The results of this analysis reveal 107 individual polymorphisms linked to phenotypic diversification, encompassing multiple molecular mechanisms. Our data suggest that the standing variation in S. cerevisiae bears an impress of selection and can be probed to understand the molecular underpinnings of evolutionary change

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