Wonderful Life Revisited: Chance and contingency in the Ediacaran-Cambrian radiation

In his 1989 book Wonderful Life Stephen Jay Gould employed the fossils of the middle Cambrian Burgess Shale to argue for a pervasive role of contingency in the history of life. But Gould wrote at the advent of an explosion of research in the Ediacaran-Cambrian diversification of animals, before ‘tree-thinking’ had made great inroads into the reconstruction of phylogeny, and with just the first glimmer of data on the remarkable conservation of developmental genes across major animal clades. More than twenty years on, not only have views of the Burgess Shale fossils undergone considerable change, but the role of contingency has become more widely accepted among paleobiologists. Yet much of Gould’s argument that if one ‘played the tape again’ the outcome would differ is difficult to accept. In this contribution I review new views of the Ediacaran-Cambrian explosion relevant to the role of chance in evolution as an example of a larger tension between historicity and laws in evolution. Introduction Although the importance of determinism versus chance was not one of the ‘eternal metaphors’ in Stephen Jay Gould’s essay of the same name (Gould, 1977), but it might well have been, for the debate over how much of the history of life is deterministic, the result of physical processes, scaling laws or various biological constraints, versus how much of it reflects either chance or just one of many possible evolutionary histories (contingency) dates at least to Darwin (Beatty, 2008). Although the topic became less prominent with the Modern Synthesis, chance and necessity served as the title of Monod’s eponymous book (Monod, 1972), arose as ‘frozen accidents’ in Crick’s early discussion of the structure of the genetic code (Crick, 1968), and played a significant role in Kauffman arguments that many aspects of evolution may be ‘frozen accidents’, preserved not for their adaptive value but rather because they generate complexity which is subsequently preserved (Kauffman, 1993). The tension between determinism and chance continues today (Carroll, 2001). It appears in discussions over the ubiquity of allometric scaling relationships (Brown et al., 2004) and in structuralist arguments for the importance of physical forces (Salazar-Ciudad et al., 2003). In astrobiology a fundamental assumption is that sufficient regularities exist in the history of life that studies on Earth will have implications for life elsewhere in the Universe. The ubiquity of convergence of morphological form has often been used as evidence against contingency (Conway Morris 2003, McGhee, 2011), generating a suite of issues. But chance and contingency are different issues. Since 1989 the much of focus of this tension over chance,