Loss of dispensable genes is not adaptive in yeast.

Abstract

A substantial share of genes identified in yeast can be deleted without visible phenotypic effects. Current debate concentrates on the possible roles of seemingly dispensable genes. The costs of maintaining unnecessary functions has attracted little attention. The hypothesis of antagonistic pleiotropy postulates that adaptations to different constituents of the environment are likely to interfere with each other, and therefore loss of unnecessary functions is potentially advantageous. We tested an entire collection of nonessential yeast gene deletions in a benign and nutritionally rich environment in which the number of dispensable genes was particularly high. We applied a series of competition experiments that could detect differences in relative fitness of approximately 0.005. No beneficial deletions were found, except perhaps for the deletion of about a dozen genes that slightly improved competitive ability; however, a functional explanation of the fitness advantage is lacking. The paucity of beneficial gene deletions is striking because genetic adaptations to laboratory conditions are regularly observed in yeast. However, it accords with the finding that the gene contents of four species of Saccharomyces are nearly identical, despite up to 20 million years of independent evolution and extensive DNA sequence divergence. Such extreme conservation of functions would be improbable if there were periods of selection promoting the loss of temporarily dispensable genes. The evident cohesion of the yeast genomes may be their evolved feature or an intrinsic property of complex genetic systems.