Developmental Plasticity and Evolution. Mary Jane West-Eberhard. Oxford University Press, New York, 2003. 794 pp., illus. $100.00 (ISBN 0195122348 cloth).
One can formalize evolution by natural selection using the equation Δz̄ = sVG /VP; that is, the change in mean phenotype of a trait across generations (Δz̄) is a function of the covariance of the trait and fitness (force of selection, s), the amount of genetic variation of the trait (VG), and the amount of phenotypic variation of the trait (VP). Mary Jane West-Eberhard posits that the Darwinian modern synthesis has focused almost exclusively on the first two elements of that triumvirate and ignored the third. Her central thesis is that the primary driving engines of evolution are the appearance of new phenotypic variation by environmental change and the plastic capacity of genomes. To support this claim, she has undertaken a 10-year effort that marshals an immense array of facts and examples (637 pages of text and about 3000 references).
This book alternately stimulated me, frustrated me, and caused me to jot copious notes in response to West-Eberhard's ideas. Such varied reactions can be expected in response to a book of this scope, which provides one of the most comprehensive, current summaries of macroevolutionary facts while putting forward new and unique ideas. West-Eberhard cuts through the thicket of terminological clutter that evolutionary biology is prone to. She often begins a chapter by summarizing the key ideas and the many terms used to present those ideas; then she presents a slimmed-down set of key terms, clearly defined, that she will use. This book is a must-read for molecular biologists, molecular geneticists, and developmental biologists for the way it dispels typological thinking. For evolutionary geneticists, this book opens up the black box of development.
The heart of the book is West-Eberhard's contention that “environmental induction is probably more important than mutation for the origin of adaptive novelties” (p. 499). This contention provides an important explanation for a major hole in modern evolutionary theory, the origin of traits. West-Eberhard's theory is that traits derive from environmentally induced plastic variation. Such new phenotypic variation becomes available to selection because “environmental inducers…are inexorably present” (p. 504). She proceeds to push this idea in as many directions as possible, some more successful than others. For example, her developmental-plasticity hypothesis of speciation is a plausible addition to current theories. Problems arise, though, in her push toward microevolution, which highlights the biggest shortcoming of this book, a failure to provide a formal version of its central thesis.
West-Eberhard opens her preface by stating that this is a book for those “interested in evolutionary theory.” Given this statement, what appears odd is that the book contains not a single equation or simulation result. Other theories are mentioned, but no details are ever provided. It only slowly dawned on me that this lack is quite deliberate and follows from West-Eberhard's contention that a gene-focused evolutionary theory is misguided. Quantitative genetics is barely mentioned, with only three entries in the index.
While West-Eberhard makes numerous predictions about how her hypothesized mechanisms would operate, all are made in a broad, hand-waving fashion. Ignored are details such as the frequency of environments and their predictability, the spatial structure of populations, and migration rates. Some of her predictions are convincing, though I am very skeptical of others. The lack of a quantitative theory is a potentially serious problem. The history of evolutionary biology is littered with examples of intuition and verbal theory shown to be wrong. For example, evolution in spatially structured populations can be quite different from that in unstructured populations. Fine-scale adaptation requires that the environmental inducers also vary on a fine scale. If they do, they cannot be omnipresent, as required for the inducers to be responsible for the origin of novel traits. The development of a quantitative theory is a challenge left by this book.
West-Eberhard fails to acknowledge the successes that the modern synthesis has achieved over the past 70 years in explaining and predicting microevolutionary processes. In making a case against the importance of mutations of small effect in gradual evolution, for example, she ignores mutation accumulation experiments that clearly demonstrate that mutation alone can account for sufficient new variation. Experiments of long-term selection in a single environment have shown the efficacy of selection fed by mutational variation.
What are the relative roles of selection, mutation (in the broad sense), and developmental potential in setting the course of evolution? Although West-Eberhard demonstrates that developmental potential can be important, we still need to determine whether it is. Complaints about adaptationism come down to contention with the general belief that selection always optimizes a trait. Theory predicts optimization, but the reality recognized by most evolutionary biologists is that the environment often changes too quickly for optimization to occur. While “fish gotta swim and birds gotta fly” (penguins excepted), one can consider these as first-order adaptations. It is the second-order term—more fine-scale adaptations—that is under debate. West-Eberhard makes a convincing case that the importance of developmental processes has been misconstrued, yet in making that case she is often guilty of making the opposite error. Her text and argument are too complex for her to be accused of dogmatism, but she often seems to overstate her case. West-Eberhard's theory is very phenocentric. While rightly criticizing genocentric theory, she ignores the merits of that theory. A complete understanding requires both.
Despite West-Eberhard's attempt to make her theory universal, the book speaks mostly to the kingdom Animalia. Plants appear only as occasional examples, except for two notable, extended discussions of the evolution of maize and CAM (Crassulacean acid metabolism), a specialized form of photosynthesis. Little attempt is made to deal with the fundamental differences in the developmental mechanisms of plants and animals (e.g., plants do not have separate somatic and germ cell lineages), and there are some odd statements, for example, about metamorphosis in plants (something that does not exist). Fungi and single-celled organisms are almost entirely absent from the book.
West-Eberhard does an excellent job of discussing the early history of many of her ideas, often tracing them back to Darwin. Such attention to historical roots is frequently absent in biology. The downside, though, is the short shrift given to the literature of the past 15 years. The lengthy gestation of this book has led to some anachronisms. At times West-Eberhard seems to be arguing against ideas that were largely abandoned decades ago, at least by those in the forefront of research on these issues (although such ideas can have a surprising longevity, continuing to circulate in adjacent fields and lodging in textbooks). What is frustrating is her failure to acknowledge the evolution of these ideas in their core disciplines. For example, she seems to believe that plasticity as an important phenomenon is ignored by evolutionary biologists. This position is belied by the 10-fold increase between 1985 and 2000 in the number of published articles that deal with this topic.
West-Eberhard's complaints about the theory of the evolution of plasticity are based on her looking at quantitative genetic descriptions and models and failing to find mechanistic answers. Some of these limitations are due to confusions at the time the models were developed, and she fails to acknowledge advances in the years since. Overall, the book lacks references to the past 15 years of theory development. The few recent articles that West-Eberhard does cite are not those that have been central in the development of contemporary theory.
A good book should spark thought and controversy; and this book accomplishes that goal. I certainly do not agree with all of the ideas put forward here, but at its core, this book contains important new ideas about the evolutionary process. It behooves anyone interested in understanding the mechanisms behind large-scale patterns of evolution to grapple with this book.
