Species crawl out of the verbal fog

The "modern synthesis" of the 1930s and 1940s produced a strong consensus on the nature of the evolutionary process among biologists in the English-speaking world. Its cornerstone was the neo-Darwinian principle that evolution largely reflects a process of stepwise change, caused by natural selection acting on genetic differences among individuals within populations. Over the past 30 years, this principle has met two major challenges. The first comes from molecular biology, with the rise of the idea that much evolutionary change in DNA and protein sequences may reflect mutations with little or no effect on fitness, which can spread through a population by random sampling events. While the role of neutral versus selectively driven molecular evolution is still an active research area, neutral evolution has been smoothly incorporated into the canon of evolutionary biology. It is, however, unlikely to play an important role in evolution at the level of morphology, physiology or behaviour, the main subject matter of the "modern synthesis".

The other challenge comes from palaeontology. The most prominent person involved was Stephen Jay Gould, who died at the age of 60 shortly before this review was written. Gould was, of course, world famous for his popular writings on science. His professional work has probably aroused more controversy over the past 30 years than that of any other evolutionary biologist. This volume is his magnum opus (literally so, weighing in at 2.3 kg). Unlike most of his books, it is aimed at an audience trained in evolutionary biology. It provides a detailed account of Gould's final judgements on his challenge to the neo-Darwinian view of evolution.

The source of controversy is the claim by Gould and some fellow palaeontologists that the processes of "macro-evolution" are distinct from "micro-evolution". Micro-evolution refers to evolutionary changes within populations of a single species, accessible to study by investigations of living species. Macro-evolution refers to events at higher taxonomic levels. The term was originally introduced by Richard Goldschmidt, who in 1940 argued that a distinct type of genetic change, involving a sudden transformation of a whole suite of characters (a "macromutation"), is involved in the origin of species and higher categories. This, of course, is completely at odds with neo-Darwinism.

The theory of evolution by punctuated equilibrium, the cornerstone of Gould's thinking, is less radical. It asserts that the prevailing pattern of evolution of morphological traits seen in the fossil record is one of little change in the characteristics of a species over long periods of evolutionary time (stasis), followed by abrupt changes associated with the formation of a new species. By new species, Gould means a population that can no longer interbreed with its ancestor, not just a morphologically distinct new form. Gould claims that evolutionary patterns above the species level involve the differential proliferation of species (species selection). He argues that this is the major force shaping the kinds of organisms that come to dominate the world in a particular period of earth history, and that success at this level has little to do with the effects of selection acting within species.

Gould also emphasises the possibility that evolutionary change is "channelled" by restrictions on the types of change that are permissible by the rules of development. He seems to regard this as having much greater significance than adaptations to similar environments for explaining cases in which very similar structures have evolved independently in different lineages. Somewhat in contradiction to this notion, he also attaches great importance to the role of contingency in the historical record of evolution. This is exemplified by the mass extinction event at the end of the Cretaceous period that wiped out whole groups of formerly dominant forms such as the dinosaurs, probably as a result of an asteroid impact. Without this random event, the present dominance of mammals on the land might never have happened.

Punctuated equilibrium has aroused controversy on two fronts. One was the question of its accuracy as a description of the fossil record. Gould argues fiercely in this book that it is accurate, and that evolution within a single lineage almost never results in a change large enough to count as a specific difference. In sharp contrast, in the recent second edition of his excellent book, Genetics, Paleontology and Macroevolution , Jeffrey Levinton has compiled data that seem to show that there is frequently considerable evolutionary change within single lineages, although its rate is often highly episodic.

The other controversy concerns the mechanisms that could generate the proposed pattern of punctuated equilibrium. Gould and his associates had earlier favoured innate constraints on evolutionary change as an explanation for stasis, and postulated unusual genetic events such as the random fixation of chromosomal rearrangements in small populations as an explanation for the sudden changes allegedly associated with species formation. Gould now concedes that he was wrong about these mechanisms. This leaves punctuated equilibrium without a firm mechanistic basis. Gould gives no convincing reasons why significant evolutionary change of the kind visible in the fossil record should be restricted to the time at which a population becomes reproductively isolated, and indeed his critics have pointed out that this is inconsistent with the evidence from studies of contemporary organisms. In fact, Gould seems uninterested in the mechanisms of evolutionary change at the level of populations. In this lengthy book, fewer than 100 pages are devoted to the formulation of these mechanisms by the architects of the modern synthesis, compared with nearly one-third devoted to 19th-century thought.

But if there is no tight association between change in morphological characters and speciation, where does this leave species selection? Most evolutionary biologists would accept that the properties of a species can affect its long-term persistence or chance of producing new daughter species. There is a question, however, as to how frequently we can assign a causal connection between the long-term survival of one group of species with a set of characteristics A, and another group with set B. Such a difference could be purely fortuitous, as Gould recognises. Until palaeontologists can come up with clear criteria for testing for species selection, as molecular evolutionists have done for selection on changes in DNA or protein sequences, the concept remains a largely speculative one, with little explanatory power.

In this book, Gould displays his characteristic erudition, ranging over a much wider variety of topics than those just discussed, with a heavy emphasis on historical questions. In my view, the book suffers from two major flaws, regardless of whether Gould is right or wrong on the points at issue. First, Gould does not discuss the arguments of his critics in any detail, often even failing to cite their papers. There is no real attempt at a balanced treatment of controversial topics, and Gould exhibits a strong tendency to attribute non-scientific motivations to proponents of views he dislikes. He uses emotionally loaded terms to make the reader sympathise with his views; one can almost hear the sneer in his voice when he refers to neo-Darwinists. In contrast, he writes warmly about unorthodox figures such as Goldschmidt, whom he compares with the hate-figure Goldstein in Orwell's Nineteen Eighty-Four , although in the end he cannot accept a role for Goldschmidtian macromutations.

Second, the book is badly written. Gould's style is pompous and repetitive, with numerous longwinded digressions and many meandering sentences that occupy nearly a page. I was constantly stumbling around in a verbal fog, and losing the thread of the argument. If Gould had stuck to the point and restrained his love of rhetorical flourishes, he would have produced a much better book, perhaps making a stronger case to have substantially modified our thinking about evolution.

Brian Charlesworth is Royal Society research professor, Institute for Cell, Animal and Population Biology, University of Edinburgh.