Evolution, the Extended Synthesis

15 - Evolution of Evolvability

15 Evolution of Evolvability Günter P. Wagner and Jeremy Draghi Over the last half century evolutionary biology has been a highly active and successful field of biological research with an increasing number of journals and online outlets supporting a rapidly growing scientific literature . Many of these publication organs have citation rates equal to or higher than many established journals in molecular biology, and thus it should not come as a surprise that our knowledge of evolution is rapidly expanding. The current understanding of evolution is much different, of greater reach and depth than either that of Darwin or that of the architects of the “Evolutionary Synthesis” from the 1950s. The fact that evolutionary biology has extended beyond that of the original Evolutionary Synthesis is therefore obvious. Of course there are different ways by which a science can expand and change. Rapid expansion of the factual knowledge base is one way that science makes progress, and another is change in the conceptual makeup of a discipline.When Massimo Pigliucci recently asked in the journal Evolution “Do we need an extended evolutionary synthesis?” he certainly had the second mode of change in mind (i.e., the question of whether the way we explain and understand evolution has changed or should change, given what we know [Pigliucci 2007]). Here we want to discuss one specific aspect of evolutionary biology that represents a break from the research tradition of the synthesis : namely, research on evolvability and its evolution. This subject is still considered by some prominent biologists as suspect (Sniegowski and Murphy 2006; Lynch 2007). Nevertheless, a PubMed search with the keyword “evolvability” yielded 236 papers on September 4, 2008; some of them refer to evolvability in a generic sense, but a large fraction also talk about evolution of evolvability. We think that the idea of evolution of evolvability is not as radical a break from the tradition of population genetics theory as some population geneticists may think. The neglect of evolution of evolvability by the research program of the synthesis 380 Günter P. Wagner and Jeremy Draghi is more a self-inflicted blind spot rather than dictated by a real limitation of the conceptual framework of population genetic theory itself. Incorporating research on the evolution of evolvability into mainstream evolutionary biology, however, can greatly enhance the conceptual reach of evolutionary biology and resolve long-standing theoretical disputes. Understanding evolvability and the evolution of evolvability can have both far-reaching conceptual and practical benefits.The most fundamental reason why research into evolvability is important for evolutionary biology is that it addresses one of the most basic assumptions of contemporary evolutionary theory: that complex organisms can arise from selection on random genetic variation.This is the part of evolutionary biology that is most consistently challenged from outside of biology,most notably by creationists. It is easy to sympathize with those whose intuition does not accommodate the idea of random variation leading to increased complexity in evolution. The reasons why most trained biologists do not have these problems is that there are good experimental and theoretical arguments why our intuition is misleading in that respect. But this body of evidence does not yet amount to a comprehensive understanding of what and how genomic and developmental features of organisms affect (positively or negatively) their ability to evolve. In particular we do not have a good understanding of how and why these features evolve (Pigliucci 2008). Intellectual honesty requires that evolutionary biologists develop a deeper understanding of evolvability and how it arose and changed during evolution. On a somewhat more specialized level, but still of fairly general importance , is the possibility that at least some features of genomic organization may have a deep connection to evolvability and the evolution of evolvability: for instance, the way cells are put together and how development is orchestrated (Rutherford and Lindquist 1998; Rutherford 2000; Gerhart and Kirschner 2007; Hendrikse et al. 2007; see also chapter 10 in this volume). These features include conserved core components used in different contexts, weak linkage among components, modularity, robustness, and many more. Many of these features are global organizational features of organisms that have not received serious consideration within evolutionary biology, which often is narrowly focused on individual traits or genes. A different aspect of the same way of thinking is Rupert Riedl’s idea that differences in body plan organization might be understood as different ways of answering the challenge of evolving complex organisms from randomly generated genetic variation...