Evolutionary tinkering with transposable elements

It was almost 30 years ago when Francois Jacob declared that evolutionary innovation (the emergence of novel form and function over time) occurred primarily via a process of “tinkering” (1). By tinkering, Jacob essentially meant the creation of novelty through random combinations of preexisting forms. Two fundamental and countervailing notions are implicit in this view of evolution: optimality versus constraint. Were evolution to perform optimally, a more apt metaphor might be that of an engineer. An engineer works according to a plan, with a precise goal for the desired end, and uses material designed specifically toward that end. Evolution, on the other hand, must work without the benefit of foresight and is subject to very real constraints with respect to the material at its disposal; as such, evolutionary biology is replete with examples of suboptimal solutions to functional challenges (2). Similarly, a tinkerer works without a clear plan by using anything and everything at his disposal to produce an entity that possesses some kind of (unanticipated) functional utility. In this issue of PNAS, Cordaux et al . (3) explore an example of tinkering along the human evolutionary lineage, whereby an existing host gene merged with a transposable element (TE) to create a primate-specific chimeric gene. In the decades since Jacob's exposition, molecular biology studies have produced a deluge of primary data (tens of thousands of three-dimensional protein structures and literally billions of nucleotides of gene sequences, including hundreds of complete genomes in the past few years alone). Comparative studies of the resulting data have underscored the extent to which genome evolution is indeed characterized by tinkering. There are a discrete and finite number of structural folds, protein sequence domains, and gene families (4); new genes evolve through slight modifications and/or recombinations of these preexisting forms. The actual de novo evolution … *E-mail: jordan{at}ncbi.nlm.nih.gov