Abstract
Researchers have long been enthralled with the idea that gene duplication can generate novel functions, crediting this process with great evolutionary importance. Empirical data shows that whole-genome duplications (WGDs) are more likely to be retained than small-scale duplications (SSDs), though their relative contribution to the functional fate of duplicates remains unexplored. Using the map of genetic interactions and the re-sequencing of 27 Saccharomyces cerevisiae genomes evolving for 2,200 generations we show that SSD-duplicates lead to neo-functionalization while WGD-duplicates partition ancestral functions. This conclusion is supported by: (a) SSD-duplicates establish more genetic interactions than singletons and WGD-duplicates; (b) SSD-duplicates copies share more interaction-partners than WGD-duplicates copies; (c) WGD-duplicates interaction partners are more functionally related than SSD-duplicates partners; (d) SSD-duplicates gene copies are more functionally divergent from one another, while keeping more overlapping functions, and diverge in their sub-cellular locations more than WGD-duplicates copies; and (e) SSD-duplicates complement their functions to a greater extent than WGD–duplicates. We propose a novel model that uncovers the complexity of evolution after gene duplication.
Highlights
The mechanisms underlying the emergence of novel functions in nature remain a mystery
We show that despite the large amount of genetic material originated by whole-genome duplication in the yeast Saccharomyces cerevisiae, these duplicates specialized in subsets of ancestral functions
The gene copies formed by small-scale duplications (SSDs) persist in the genome if their products do not upset the stoichiometric balance (Figure 1A) or the positive effects on fitness owing to the genetic robustness provided by a second gene copy compensates negative fitness effects of dosage imbalance
Summary
The mechanisms underlying the emergence of novel functions in nature remain a mystery. Most Angiosperms have undergone at least one genome duplication (polyploidy) [2,3] in the Creataceous era, contemporary with the explosion of plant metabolic and physiological diversity [4,5] This diversity resulted from the expansion of protein families by gene duplication, including pepsin- and subtilisin-like proteases [6], metacaspases [7], regulatory genes [8] and developmentally important MADSBox genes [9,10,11,12]. It is tempting to establish a link between gene duplication and biological complexity, but the mechanisms underlying the persistence of genes in duplicate and determining their functional fate remain largely obscure
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