Re) structuring Darwinism

The Structure of Evolutionary Theoryby Stephen J. GouldHarvard University Press, 2002. £27.50 hbk (1464 pages) ISBN 0674006135What does it mean to be a Darwinian? One certainly can be an evolutionist without being a Darwinian. After all, Darwin's own grandfather had written musings on evolution. Even the idea of natural selection is not unique to Darwin; it having been articulated independently by several nineteenth century naturalists.In The Structure of Evolutionary Theory, published shortly before his death in May 2002, Stephen J. Gould identifies the essence of Darwinism as consisting of three statements about the nature of natural selection: its agency, its efficacy and its scope. The first criterion (agency) is that the individual organism is the primary agent of selection. Selection operates on individual organisms. Under the second criterion (efficacy), natural selection not only eliminates the ‘unfit’, but is also the primary creator of adaptations and novelties. It creates ‘by slowly accumulating the positive effects of favorable variations through innumerable generations’ (p. 14). The third criterion (scope) is that the natural selection results not only in changes on a microevolutionary level but also, by extrapolation, explains the full pageantry of life.This intimidatingly long book is, in a sense, two (still long and comprehensive) volumes united by the common theme of exploring this Darwinian tripod. The first ‘volume’ is an account of the historical development and the challenges made to each of the Darwinian criteria before the middle decades of the twentieth century when the modern evolutionary synthesis was formulated. Darwin and the architects of the evolutionary synthesis saw variations as being copious, minute in size and undirected. Theories that challenged Darwinism usually challenged at least one of Darwin's precepts about variation. For instance, several theories, generally called orthogenesis, were proposed wherein variation is directed along channels of internal constraint. Proponents of orthogenesis varied with regard to how much power they attributed to natural selection, but most saw it as a weak force. Starting with the mathematical theory of the population geneticists, Mendelian genetics and Darwinian evolution would be fused in the evolutionary synthesis. Gould argues that this synthesis was not just a synthesis, but also a constriction. In the early, more pluralistic synthesis of the 1930s and 1940s, orthogenesis and other challenges to natural selection were marginalized. Gould saw that early synthesis as a positive development. Later, the synthesis would harden. Gould believes that this hardening went too far in asserting the seemingly all-encompassing power of natural selection and dismissing alternatives.The historical chapters are worth reading for many reasons, not the least of which is that Gould adroitly demonstrates how the same debates (e.g. functionalism versus formalism) have persisted in new guises over the past two centuries. He also implies that the first decade of the century of genetics, at least on the surface, is remarkably similar to our own times, the first decade of the century of genomics.In the contemporary section, Gould presents himself as a radical Darwinian. Although remaining within the Darwinian framework, he proposes radically restructuring of each of the legs of the Darwinian tripod. In contrast to the nineteenth century critics of Darwin who typically relegated natural selection to the minor role of ‘a reaper of the unfit’, Gould wants to extend orthodox Darwinism by supplementing natural selection with auxiliary mechanisms. These auxiliary mechanisms include the selection of species and other higher-level individuals, internal constraints posed by developmental pathways and mass extinctions. Gould envisions a middle path, wherein natural selection is neither ‘die Allmacht’ (the Omnipotent) of the ultra-Darwinian August Weismann and the c.1959 synthesis, nor is it ‘die Ohmacht’ (the Impotent) of the orthogeneticist Theodore Eimer.The limited space provided prohibits a detailed critical review of a book of such scope and nuance as Gould's. Instead, I focus on the aspect of Gould's book of greatest interest to the TiG readership – the implications of the evolution of development (evo–devo) studies.Arguably, the most important theme emerging from the recent evo–devo synthesis is the striking conservation of genes and genetic pathways across animals that are separated by over 500 million years of evolution [1.xRaff, R.A. See all References, 2.xWilkins, A.S. See all References]. This phenomenon, which Gould calls ‘deep homology’, was not predicted by the evolutionary synthesis. The adherents of strict Darwinism during the peak of the narrowing of the synthesis would expect the power of natural selection to erode away the signature of common descent. Indeed, Gould presents (several times) a quote by Ernst Mayr:‘In the early days of Mendelism there was much search for homologous genes that would account for such similarities. Much that has been learned about gene physiology makes it evident that the search for homologous genes is quite futile except in very close relatives.’ (Ref. [3xMayr, E. See all References][3] p. 609)To Gould, Mayr's statement illustrates how the ‘hardening adaptationism can suppress interesting questions’ (p. 539). Under the extreme adaptationism of late synthesis, independent evolution by natural selection should erode the genetic homology across such disparate groups. Yet, not only are the same genes that determine segmentation in insects also found in vertebrates, but they also function in very similar ways in these vastly different animals.Gould proceeds to use various cases of parallelism (independent evolution of similar features in different lineages) to demonstrate how these shared developmental pathways can constrain evolutionary directionality. Thoracic feeding limbs called maxillipeds have evolved independently in many lineages within Crustacea. Gould cites studies showing that across these independent lineages, in those segments where activity of the Hox genes Ubx and abdA is suppressed, maxillipeds form.Gould concludes in celebrating the ‘…initially surprising example of the unanticipated durability of ancient genetic pathways, and of their continuing power to constrain the subsequent phylogeny of life along broad and fruitful (but still limited) routes of wonderfully diverse, but historically rule-bound, adaptive designs.’ (p. 1116–1117).A study published shortly after publication of The Structure of Evolutionary Theory, suggests another manner in which internal factors arising from developmental pathways can produce a phenomenon conventionally believed to be due to natural selection. Canalization, the buffering of the phenotype from environmental and/or mutational insult, has been generally put forth as a textbook example of the power of stabilizing selection. Not only can selection directly maintain phenotypes, but it can do so indirectly via canalization. Although stabilizing selection certainly will promote canalization, Siegal and Bergman [4xWaddington's canalization revised: developmental stability and evolution. Siegal, M.L. and Bergman, A. Proc. Natl. Acad. Sci. U. S. A. 2002; 99: 10528–10532Crossref | PubMed | Scopus (337)See all References][4] show that it might not be necessary for it as canalization can arise from general properties of genetic networks.In addition to the chapter on constraints arising from shared developmental genetic pathways, I also highly recommend Gould's chapter ‘Species as Individuals in the Hierarchical Theory of Speciation’. Here, Gould presents a spirited defense of species having attributes of Darwinian individuals. He then presents a hierarchical selection theory showing the similarities and differences of each of the levels of selection. Although agreeing with strict Darwinians that adaptation is primarily owing to selection on organisms, Gould states that other features of the pageantry of life are influenced more by selection operating on species.Yes, this is an indulgent book. Yes, more editing would have been improved it. A reasonable reader can disagree with validity or generality of some of the conclusions Gould reaches. One can also disagree with Gould about how radical his conclusions are. But despite its flaws, The Structure of Evolutionary Theory is a magisterial work that ought to be read and discussed for decades to come.