Evolution: A View from the 21st Century

Evolution: A View from the 21st Century, written by an eminent microbiologist–bacterial molecular geneticist, is an ambitious book. It has something novel and highly interesting to say about evolution and it deserves to be widely read. Nevertheless, I have found doing this review a difficult exercise. In the interest of ‘‘full disclosure,’’ I should say that the author, Jim Shapiro, is a friend with whom I have previously discussed these ideas. (I had not, however, known about the book until it was published.) Friends, however, do not always agree and he and I have differed about some of his ideas. Nor have those disagreements been dispelled by my reading the book. In particular, I think that there is an alternative interpretation of some of the phenomena presented and cited here as providing support for the central thesis. In addition, I regard one core proposition, though only explicitly stated at the end and then partially hedged, as, simply, wrong. Hence, although I strongly recommend the book and hope that it is widely read and discussed, I cannot equivalently endorse its big idea or, at least, not all of it. In this review, I will first describe the contents of the book and its central thesis and will then try to explain where the problems, in my opinion, reside. A few words first, however, about the author and his pathway into evolution from bacterial molecular genetics, might be appropriate. Jim Shapiro was, as a postdoc in Jonathan Beckwith’s lab in 1969, the first person to purify a small set of protein-coding genes, those of the lac operon (which had been imbedded in a much larger set of phage genes within transducing phages). The strategy was brilliant but was not applicable to most genes, hence, it was superseded by the more general cloning techniques for specific genes that came to the fore in the early 1970s. Nevertheless, it was a milestone in the development of the modern (post60s) form of molecular biology, involving DNA sequence isolation and characterization. Even more significantly, Jim had, as a postdoc with Francois Jacob, the preceding year, discovered that certain mutations in Escherichia coli were due to insertions of bacterial transposable elements, the so-called insertion sequence (IS) elements. The discovery immediately made geneticists aware that the transposable element phenomenon, discovered by Barbara McClintock in maize two decades earlier but dismissed as an oddity by most geneticists, was, almost certainly, a general one, with major implications for mechanisms of gene control, biological development, and evolution (Bukhari et al. 1977). That work eventually led on to a 12-year friendship between Jim and Barbara McClintock, which lasted until her death. In that friendship and exchange of ideas lay the seeds of Jim’s interest in evolution—the major focus of McClintock’s attention in the last decades of her life—and, ultimately, in the thesis developed in this book. The key goal of this book is to demonstrate that a central premise of Darwinian evolution is incorrect and to spell out the implications of that conclusion for evolutionary theory. The Darwinian premise is that genetic variations—‘‘mutations’’ including chromosomal breaks and rearrangements) in current terminology but ‘‘hereditary variations’’ in Darwin’s—occur ‘‘randomly,’’ that is, irrespectively of environmental conditions and adaptive ‘‘need.’’ (Darwin actually equivocated somewhat on this point, at times endorsing the inheritance of acquired characteristics, but he seemed aware that the strong form of his theory required that variations arise by chance, i.e., without respect to future utility, hence randomly.) This central plank of classic Darwinian evolution is also embedded, according to Jim and several others, in a more recent formulation, namely Francis Crick’s ‘‘central dogma,’’ first stated in 1958, and reiterated and (basically reaffirmed) by Crick in 1970. This is the idea that ‘‘information’’ flows one-way from nucleic acids (DNA and RNA) to proteins and never in the reverse direction. From this, Jim argues that it is tantamount to the statement that environmental influences never influence DNA structure and information content; the flow of ‘‘instruction’’ is always one-way, outwards from DNA to proteins and thence to biological properties. (His formulation of this view is that it treats the genome as a ‘‘read only memory’’ storage system.) Whether that extrapolation from Crick’s statement is truly fair is something best left to historians of science. In neither statement, to my eye, was Crick explicitly considering the kinds of organismal response that can alter genomic