Abstract
The number of chromosome sets contained within the nucleus of eukaryotic organisms is a fundamental yet evolutionarily poorly characterized genetic variable of life. Here, we mapped the impact of ploidy on the mitotic fitness of baker's yeast and its never domesticated relative Saccharomyces paradoxus across wide swaths of their natural genotypic and phenotypic space. Surprisingly, environment-specific influences of ploidy on reproduction were found to be the rule rather than the exception. These ploidy–environment interactions were well conserved across the 2 billion generations separating the two species, suggesting that they are the products of strong selection. Previous hypotheses of generalizable advantages of haploidy or diploidy in ecological contexts imposing nutrient restriction, toxin exposure, and elevated mutational loads were rejected in favor of more fine-grained models of the interplay between ecology and ploidy. On a molecular level, cell size and mating type locus composition had equal, but limited, explanatory power, each explaining 12.5%–17% of ploidy–environment interactions. The mechanism of the cell size–based superior reproductive efficiency of haploids during Li+ exposure was traced to the Li+ exporter ENA. Removal of the Ena transporters, forcing dependence on the Nha1 extrusion system, completely altered the effects of ploidy on Li+ tolerance and evoked a strong diploid superiority, demonstrating how genetic variation at a single locus can completely reverse the relative merits of haploidy and diploidy. Taken together, our findings unmasked a dynamic interplay between ploidy and ecology that was of unpredicted evolutionary importance and had multiple molecular roots.
Highlights
A central yet poorly understood variable of life is the number of chromosome sets contained within the nucleus of eukaryotic cells
Organisms vary in the number of chromosome sets contained within the nucleus of each cell, but neither the reasons nor the consequences of this variation are well understood
We designed yeasts that differed in the number of chromosome sets but were otherwise identical and mapped the consequences of such ploidy variations during exposure to a large palette of environments
Summary
A central yet poorly understood variable of life is the number of chromosome sets contained within the nucleus of eukaryotic cells. Mutational models are based on chromosome set additions increasing the number of mutable sites but masking recessive variation, thereby affecting the emergence, tolerance to and purging of de novo mutations [11] Factors such as strength of selection, mutation rate, population size and ratios of deleterious to adaptive and recessive to dominant mutations determine whether a particular ecological context will favor high or low ploidy [10,12,13,14]. Cell size models presuppose higher ploidy states to increase cell and organelle volume but to fail to proportionally enlarge surface areas [15], thereby distorting the balance between transport rates, costs and needs. This potentiates co-selection on ploidy and ability to mate, outbreed and sporulate in response to mostly unknown environmental cues
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