Tinkering loci: genomic hotspots of gene birth and evolutionary innovation

How does evolution create new things? A key strategy is 'tinkering': changing and re-using existing biological components in new ways. Tinkering is generally thought to be genomically unpatterned, occurring without spatial or other kinds of structure. Here, I find that 'tinkering loci,' kilobase-scale regions with significantly higher rates of gene birth by tinkering, are common in Drosophila genomes. These regions work by accumulating unusually high concentrations of duplicated gene fragments from around the genome, increasing the rate at which they can be co-opted to create new genes, especially ones containing new combinations of previously unrelated pieces. Their activity varies on timescales of a few million years; they use a universal mechanism enabled by all major kinds of transposable elements; and they form networks to collectively innovate and enable their useful products to duplicate into gene families. Tinkering loci demonstrate that evolutionary innovation can be a property of genome architecture and suggest a tunable mechanism shaping the tempo and mode of animal evolution.