Pervasive and Persistent Redundancy among Duplicated Genes in Yeast

Abstract

The loss of functional redundancy is the key process in the evolution of duplicated genes. Here we systematically assess the extent of functional redundancy among a large set of duplicated genes in Saccharomyces cerevisiae. We quantify growth rate in rich medium for a large number of S. cerevisiae strains that carry single and double deletions of duplicated and singleton genes. We demonstrate that duplicated genes can maintain substantial redundancy for extensive periods of time following duplication (∼100 million years). We find high levels of redundancy among genes duplicated both via the whole genome duplication and via smaller scale duplications. Further, we see no evidence that two duplicated genes together contribute to fitness in rich medium substantially beyond that of their ancestral progenitor gene. We argue that duplicate genes do not often evolve to behave like singleton genes even after very long periods of time.

Author Summary

Gene duplication is the primary source of new genes. To persist, duplicated genes must lose some of the original redundancy either by partitioning the ancestral function (subfunctionalization) or by gaining new non-redundant functions (neofunctionalization). The extent to which these processes shape the evolution of duplicated genes over long periods of time is unknown. We investigate these questions experimentally by building strains carrying single and double gene deletions of duplicated genes and measuring their growth rates in rich medium. Using these data, we determine that many duplicated genes are functionally redundant to a substantial degree. We also investigate how often duplicated genes gain new functionality. We demonstrate that the fitness effects of double deletions of duplicate genes are indistinguishable from our best estimate of the fitness effects of deletions of their ancestral singleton genes. We therefore argue that many duplicate genes do not gain substantial new functionality at least in the rich medium. Our results suggest that subfunctionalization does not generally proceed to completion, even after very long periods of time, and that neofunctionalization is either rare or of little consequence, at least under some growth conditions.