The Rarity of Evolutionary Innovation through Gene Shuffling

Among three sources of evolutionary innovation in gene function - point mutations, gene duplications, and recombination among dissimilar genes (gene-shuffling)- recombination is the most potent one. However, surprisingly little is known about its incidence on a genome-wide scale. Using the complete genomes of seventeen organisms, we estimate the incidence of gene shuffling in the three domains of life, eukaryotes, eubacteria, and archea. We find that successful gene shuffling is very rare. For example, fewer than 48 successful gene shuffling events may have occurred in the genome of the fruit fly D. melanogaster since its common ancestor with the worm C. elegans more than half a billion years ago. The rate of gene shuffling is roughly an order of magnitude smaller than the rate of single gene duplication in eukaryotes, but it can approach or even exceed the duplication rate in prokaryotes. If true in general, this pattern suggests that gene shuffling has not played a major role in the many innovations that characterize the evolution of higher organisms. It also casts into doubt the notion that introns facilitate gene shuffling, because prokaryotes show an appreciable incidence of gene shuffling despite their lack of introns.