The frailty of adaptive hypotheses for the origins of organismal complexity
Michael Lynch *
Department of Biology, Indiana University, Bloomington, IN 47405
The vast majority of biologists engaged in evolutionary studies interpret virtually every aspect of biodiversity in adaptive terms. This narrow view of evolution has become untenable in light of recent observations from genomic sequencing and population-genetic theory. Numerous aspects of genomic architecture, gene structure, and developmental pathways are difficult to explain without invoking the nonadaptive forces of genetic drift and mutation. In addition, emergent biological features such as complexity, modularity, and evolvability, all of which are current targets of considerable speculation, may be nothing more than indirect by-products of processes operating at lower levels of organization. These issues are examined in the context of the view that the origins of many aspects of biological diversity, from gene-structural embellishments to novelties at the phenotypic level, have roots in nonadaptive processes, with the population-genetic environment imposing strong directionality on the paths that are open to evolutionary exploitation.
adaptation genome evolution evolvability modularity population genetics
Although biologists have always been concerned with complex phenotypes, the matter has recently become the subject of heightened speculation, as a broad array of academics, from nearly every branch of science other than evolutionary biology itself, claim to be in possession of novel insights into the evolution of complexity. The claims are often spectacular. For example, Kirschner and Gerhart (1) argue that evolutionary biology has been “woefully inadequate” with respect to understanding the origins of complexity and promise “an original solution to the long-standing puzzle of how small random genetic change can be converted into complex, useful innovations.” However, this book and many others like it (e.g., refs. 2–5) provide few references to work done by evolutionary biologists, making it difficult to understand the perceived areas of inadequacy, and many of the ideas promoted are known to be wrong, making it difficult to appreciate the novelty. Have evolutionary biologists developed a giant blind spot; are scientists from outside of the field reinventing a lot of bad wheels; or both?
Evolutionary biology is treated unlike any science by both academics and the general public. For the average person, evolution is equivalent to natural selection, and because the concept of selection is easy to grasp, a reasonable understanding of comparative biology is often taken to be a license for evolutionary speculation. It has long been known that natural selection is just one of several mechanisms of evolutionary change, but the myth that all of evolution can be explained by adaptation continues to be perpetuated by our continued homage to Darwin's treatise (6) in the popular literature. For example, Dawkins' (7–9) agenda to spread the word on the awesome power of natural selection has been quite successful, but it has come at the expense of reference to any other mechanisms, a view that is in some ways profoundly misleading. There is, of course, a substantial difference between the popular literature and the knowledge base that has grown from a century of evolutionary research, but this distinction is often missed by nonevolutionary biologists.
The goal here is to dispel a number of myths regarding the evolution of organismal complexity (Table 1). Given that life originated from inorganic matter, it is clear that there has been an increase in phenotypic complexity over the past 3.5 billion years, although long-term stasis has been the predominant pattern in most lineages. What is in question is whether natural selection is a necessary or sufficient force to explain the emergence of the genomic and cellular features central to the building of complex organisms.