Review of The Major Transitions in Evolution Revisited, edited by Brett Calcott and Kim Sterelny, Vienna Series in Theoretical Biology, MIT Press, 2011 (ISBN 978–0-262–01524-0).
Theoretical evolutionary biology has been going through both a Renaissance and an expansion over the past several years, and some of the most intriguing contributions have come from the Vienna Series published by MIT Press. Although the classical view is that population genetics theory is the centerpiece of any theoretical biology (e.g., Lynch 2007), an expanded concept of what it means to do theory in biology has been proposed (Pigliucci 2008), of which population and quantitative genetics represent but a small (if very important) component. The volume recently edited by Brett Calcott and Kim Sterelny—interestingly, both philosophers of science—picks up where the now classic volume on evolutionary transitions by Maynard-Smith and Szathmary (1997) left off and attempts to see where we are when it comes to the really big picture in evolutionary theory.
As it is typically the case with such edited volumes, the goals the editors set up to accomplish are necessarily only partially achieved, because each contributor is more or less free to roam afar from the main topic of discussion, sometimes in areas whose logical link with the topic at hand is tenuous at best. Nonetheless, there is much food for thought in this book, which would make for an extraordinarily interesting graduate-level seminar, especially if accompanied by the original Smith-Szathmary volume. (Ironically, one of the farthest afield excursions is due to Szathmary himself, who was called to comment at the end on the entire volume and instead chose to pursue—with his coauthor, Chrisantha Fernando—an only very partially related line of inquiry having to do with applying evolutionary principles to the functioning of the human brain.)
I must admit of never having been too fond of the idea of “major transitions,” understood as a somewhat coherent set of phenomena that in some meaningful way admit similar underlying explanations. The editors of this volume write that “Among the major transitions are episodes of the creation of new kinds of evolutionary agent: eukaryotic cells; multicelled animals; social insects” (p. 3). Well, perhaps, but this opens up the Pandora box of what counts as an “evolutionary agent,” and why some transitions do not seem to create new kinds of agents (the origin of language for instance). Perhaps more appropriately, Calcott and Sterelny focus on three themes that do seem to underlie the Smith-Szathmary volume, and that get major booking in this new collection: the expansion of hereditary mechanisms; the evolution of new levels of biological individuality; and the generation of variation. These are arguably some of the major issues in evolutionary biology, and they have received only partial and largely unsatisfactory treatment within the now more than half century old framework of the Modern Synthesis (Pigliucci and Muller 2010).
Although much debate is still going on about all three issues highlighted by Calcott and Sterelny, it seems beyond reasonable question at this point that: (1) hereditary mechanisms have been evolving and expanding, from the relative simplicity of the RNA world to the modern panoply of genetic, epigenetic, behavioral, and cultural inheritance (Jablonka and Lamb 2005); (2) we cannot do evolutionary theory without a serious understanding of multilevel selection, pace historical disagreements on old fashioned and new fangled group selection (Okasha 2006); and (c) the way in which variation is generated itself evolves in interesting ways, a concept captured under the general heading of “evolvability” (e.g., Woods et al. 2011). The real challenge is to make sense of these and many other related ideas within a coherent conceptual framework.
One of the people that has recently come closest to achieving this synthesis is Peter Godfrey-Smith (also one of the contributors to the Vienna volume, see Chapter 4). In his Darwinian Populations and Natural Selection (Godfrey-Smith 2009) he begins from Richard Lewontin's famous redescription of the minimum conditions for natural selection and arrives at a general framework that describes Darwinian populations as populations of agents that reproduce, without equal prospect of success, so that their descendants resemble them. Godfrey-Smith cashes out the idea in terms of an elegant graphic description—the “Darwinian space”—that he uses to situate paradigmatic and marginal cases of Darwinian evolution. For instance, three of the various dimensions that characterize a Darwinian space are the degree of fidelity of the inheritance system(s), the extent to which differences in realized fitness in a population depend on differences in the intrinsic character of the members of the population (p. 68), and the smoothness of the fitness landscape. Using these three dimensions, Godfrey-Smith presents a clear and coherent distinction among paradigmatic cases of evolution by natural selection, drift, marginal cases of Darwinian populations, evolution on rugged landscapes, and “error catastrophes.” It takes some investment to wrap one's mind around the logic proposed by Godfrey-Smith, but the effort pays off very handsomely, and the chapter included in this collection is a nice précis to his larger volume. As a bonus, this approach also provides the community with what I think is a much better way of thinking of evolution than the by now standard talk of Dawkins-style “replicators.”
What about evolvability? The chapter by Sterelny—whose framework is in fact related to that of Godfrey-Smith, and which Sterelny has used before to explore the implications of multiple channels of inheritance—provides a nice way to connect the topic of major transitions to that of evolvability and its own evolution. Sterelny explores the conditions for what he calls an enriched Darwinian environment, one that permits a better grasp of why some lineages appear to be better than others at evolving complex novel phenotypes. This work essentially lays out the conditions for evolvability to evolve, and connects the topic to those of phenotypic plasticity and of the often neglected interaction between the developmental properties of individuals and the properties of evolving populations. It is by now common, although still far from universal, to invoke most or all of the above concepts (developmental systems, multiple channels of inheritance, evolvability, plasticity, etc.) in vanguard discussions of evolution. But it is still very rare indeed to find a lucid account of how they are connected, and the one by Sterelny ought to provide much food for thoughtful discussion to anyone interested in making sense of modern evolutionary theory.
There is another aspect of current evolutionary biology that is in need of a dramatic correction: the persisting attitude to focus on (certain) animal species as objects of study, despite the fact that there are many other varied forms of life (plants, microorganisms) that are just as interesting, and arguably more crucial to our understanding of the biosphere and its history. The Calcott-Sterelny volume aptly reserves an entire section to prokaryotes—themselves of course a surprisingly heterogeneous category, as we have been increasingly appreciating over the past several years. This is a much needed attempt at shifting perspective considering that, as the editors put it (p. 101), “The evolution of multicelled plants and animals is … just a couple of late-evolving side branches in one domain of the history of life.” And yet, as again noted by Calcott and Sterelny, microbiology has historically had the same difficulty as paleontology in being accepted at the “high table” of evolutionary discourse (Prothero 2009), with the result that evolutionary theory is that much poorer for it.
That said, the Vienna volume also devotes an entire section to the understanding of developmental cycles, arguably the main feature that distinguishes uni- from multicellular organisms, and one that raises complex questions relating to the origin and maintenance of division of labor. This is of course one of the quintessential evolutionary transitions, to explain which several authors—including Samir Okasha, who has contributed to this volume—have invoked a crucial role for multilevel selection. In particular, the distinction has been made between Multi-Level Selection (MLS) 1 and MLS-2 (Damuth and Heisler 1988): in MLS-1 the focus is on the lower level units that are part of given ensembles (e.g., genes within individual organisms), whereas in MLS-2 the focus is on the ensemble itself (e.g., the organisms). Several major transitions, and in particular the one between uni- and multicellularity, can then be recast as problems concerned with shifting from MLS-1 to MLS-2, that is, from selection focusing on the lower level units to selection focusing on the higher level units—via the generation of some degree of cohesiveness that reduces the independence of the lower level units and increases the coherence of the higher level ones. Although the fitness of the lower level units in both cases is simply the expected number of new units produced at that level, the concept of fitness of the “group” or ensemble changes: in MLS-1, it is given by the average fitness of the component lower units; in MLS-2, it is given by the number of groups being produced in the next generation. Okasha and others have shown under what circumstances one can expect a shift from MLS-1 to MLS-2, and therefore what needs to happen for lower level to upper level transitions to occur.
It should be noted that, contra to popular statements, this entire approach to evolutionary reasoning—from multilevel selection theory to evolvability to the idea of major evolutionary transitions—is novel and most certainly cannot reasonably be thought to be a simple application of the well-established principles of the Modern Synthesis. This, of course, does not mean that evolutionary theory is in crisis, pace the creationists and their Intelligent Design proponent cousins. On the contrary, arguably evolutionary biology has never been such a vibrant field of scientific inquiry, characterized by breathtaking empirical work and even more dizzy theoretical advances. One would not know much about that, however, from perusing either most popular treatments of evolution aimed at the general public or even undergraduate and graduate textbooks directed to the serious student of biology. Perhaps this is to some extent unavoidable, but in a world where scientific communication is expanding via a myriad new channels and media, it is a shame that only the few people who read advanced works such as the Calcott-Sterelny volume will get a sense of the excitement in the field. If there is one improvement that I would recommend to the editors of the Vienna Series in Theoretical Biology it is to come up with the occasional companion volume that will expand the circle of knowledge to both excite the potential next generation of professionals and inspire the public. For now, however, professionals should take the time to read this material, it will be well worth the investment.