Lynch, M., Field, M.C., Goodson, H.V., Malik, H.S., Pereira-Leal, J.B., Roos, D.S., Turkewitz, A.P., and Sazer, S. (2014) Evolutionary cell biology: Two origins, one objective. Proc. Natl. Acad. Sci. (USA) 111:16990–16994. [doi: 10.1073/pnas.1415861111]Here's the bit on random genetic drift. It will be of interest to readers who have been discussing the importance of drift and natural selection in a previous thread [How to think about evolution].
Do you think Lynch et al. are correct? I do. I think it's important to emphasize the role of random genetic drift and I think it's true that most biochemists and cell biologists are stuck in an adaptationist mode of thinking.
A commonly held but incorrect stance is that essentially all of evolution is a simple consequence of natural selection. Leaving no room for doubt on the process, this narrow view leaves the impression that the only unknowns in evolutionary biology are the identities of the selective agents operating on specific traits. However, population-genetic models make clear that the power of natural selection to promote beneficial mutations and to remove deleterious mutations is strongly influenced by other factors. Most notable among these factors is random genetic drift, which imposes noise in the evolutionary process owing to the finite numbers of individuals and chromosome architecture. Such stochasticity leads to the drift-barrier hypothesis for the evolvable limits to molecular refinement (28, 29), which postulates that the degree to which natural selection can refine any adaptation is defined by the genetic effective population size. One of the most dramatic examples of this principle is the inverse relationship between levels of replication fidelity and the effective population sizes of species across the Tree of Life (30). Reduced effective population sizes also lead to the establishment of weakly harmful embellishments such as introns and mobile element insertions (7). Thus, rather than genome complexity being driven by natural selection, many aspects of the former actually arise as a consequence of inefficient selection.
Indeed, many pathways to greater complexity do not confer a selective fitness advantage at all. For example, due to pervasive duplication of entire genes (7) and their regulatory regions (31) and the promiscuity of many proteins (32), genes commonly acquire multiple modular functions. Subsequent duplication of such genes can then lead to a situation in which each copy loses a complementary subfunction, channeling both down independent evolutionary paths (33). Such dynamics may be responsible for the numerous cases of rewiring of regulatory and metabolic networks noted in the previous section (34, 35). In addition, the effectively neutral acquisition of a protein–protein-binding interaction can facilitate the subsequent accumulation of mutational alterations of interface residues that would be harmful if exposed, thereby rendering what was previously a monomeric structure permanently and irreversibly heteromeric (8, 36–39)1. Finally, although it has long been assumed that selection virtually always accepts only mutations with immediate positive effects on fitness, it is now known that, in sufficiently large populations, trait modifications involving mutations with individually deleterious effects can become established in large populations when the small subset of maladapted individuals maintained by recurrent mutation acquire complementary secondary mutations that restore or even enhance fitness (40, 41).
1. Note the brief description of how irreversibly complex structures can evolve. This refutes Michael Behe's main point, which is that irreversibly complex structures can't have arisen by natural processes and must have been designed. We've known this even before Darwin's Black Box was published.