Environment, Development, and Evolution: Toward a Synthesis. Brian K. Hall, Roy D. Pearson, and Gerd B. Müller, eds. MIT Press, Cambridge, MA, 2003. 304 pp., illus. $45.00 (ISBN 0262083191 cloth).
Ryuichi Matsuda was an insect biologist both ahead of and behind his times. This book, a tribute to Matsuda and his ideas, came from a workshop in 1996 and is very much in the same vein. Matsuda was born in 1920 in Japan; earned a bachelor's degree from Kyushu University in 1950; received his PhD in entomology from Stanford University, working with G. F. Farris; and then spent time at both the University of Kansas and the University of Michigan before moving to the Biosystematics Research Institute of Canada in 1968, where he remained until his death in 1986. At that time he was finishing Animal Evolution in Changing Environments, with Special Reference to Abnormal Metamorphosis (1987, John Wiley and Sons).
I confess that I was not familiar with Matsuda and his work before reading Environment, Development, and Evolution. My appreciation of him comes from the descriptions of his life and work by various contributors to this volume, the best of which is the brief, but personal, recollection of Mary Jane West-Eberhard, who first met him when she was a graduate student at the University of Michigan. My comments about his work are based on what I could glean from these indirect sources.
Matsuda was interested in the evolution of form, especially of insects. He recognized much earlier than most that the environment could play a large and creative role in that process. During the 1960s, few evolutionary biologists and even fewer developmental biologists appreciated this fact and the other ideas that Matsuda eventually called “pan-environmentalism.” West-Eberhard sums up Matsuda's reaction to this lack of appreciation:
Matsuda may have been hindered in his quest for a synthesis by his annoyance with neo-Darwinism. At least that attitude compromised his ability to communicate effectively with those most likely to be interested in his ideas, some of them apt to be alienated rather than convinced by terms like “neo-Lamarckianism” or even “genetic assimilation.” But Matsuda was about twenty years ahead of his audience in thinking about development and evolution, and it is a great pity that he did not live to see his ideas appreciated as they are in this book. (p. 116)
Unfortunately, some of Matsuda's defenders in Environment, Development, and Evolution seem to share his attitude. The first third of the book reads like a 20-year-old text fighting a 50-year-old battle. Roy Pearson, R. G. B. Reid, and especially Eugene Balon attempt to portray evolution as a theory in crisis and Matsuda as its savior, but their presentation is both a caricature of evolutionary theory and severely out of date. Their central claim is that evolutionary theory (“neo-Darwinism”) ignores the pervasive effects of the environment. Yet I learned as a student nearly 30 years ago that phenotypic variation among individuals in a population can be partitioned: Vp = VE + VG + VG × E + Ve + Cov(E,G), where VE is the variation due to environmental effects, VG is the variation due to genetic effects, VG x E is the variation due to differences among genotypes in how they react to the environment, Ve is variation due to developmental noise, and Cov(E,G) is variation due to the nonrandom distribution of individuals among environments. Admittedly, all of the terms with “E” in them were mostly, but not entirely, ignored until the 1980s. Since then, however, numerous papers dealing with the empirical existence and theoretical implications of these factors have appeared. Indeed, hundreds of papers are now published each year on phenotypic plasticity and reaction norms. The past decade has seen a score of books and major reviews on these subjects. Nevertheless, the authors of these opening chapters write as if this spate of research had not been carried out.
Pearson, Reid, and Balon do lay out the components of Matsuda's theory, but one problem with the way they frame the argument is that no evolutionary biologist that I know would call herself a “neo-Darwinian.” We are all just evolutionary biologists. Reid, at least, recognizes the rhetorical folly of argument by label. More important, the theory as presented is empty. The central tenet of pan-environmentalism is that the environment affects the phenotype of individuals. This principle is so obviously true that no evolutionary biologist would dispute it. However, the theory as presented goes little beyond that claim, although it is the details of how those effects occur that matter. For example, if the environment is strictly random, the effects on evolutionary processes will be very different than they would be if the environment were completely predictable. Over the past 20 years, an entire domain of evolutionary theory has arisen that deals with these issues, namely, plasticity theory—the evolution of development under environmental uncertainty. None of that theory is referenced here. (What is referenced, however, by Balon, is Michael Behe's Darwin's Black Box, which is cited as proof of the failure of evolutionary theory; apparently Balon fails to appreciate that Behe is a creationist and a proponent of intelligent design.)
I also find incongruous Pearson, Reid, and Balon's claim that pan-environmentalism is a universal theory of evolution. As presented in their chapters, this theory apparently applies only to Kingdom Animalia, and primarily to Phyla Chordata and Arthropoda. Even within those bounds, the theory seems to deal mostly with morphology and the timing of a few critical life history events, such as metamorphosis and the onset of reproduction.
The book does have some strong points. The best parts are the chapters dealing with evolution and metamorphosis in fish, herptiles, and insects. Most of these are written by people who were unfamiliar with Matsuda's work or who came upon it after his death. The chapter by John Youson on fish metamorphosis—at 40 pages, one of the longest in the book—shows clearly how Matsuda's views fit into modern ideas of plasticity and the evolution of development. The chapter is primarily a review of Youson's own work on lampreys, but Youson repeatedly links this work back to Matsuda's key ideas. Marvalee Wake's chapter on the evolution of viviparity makes a similar effort. Other chapters, such as the one by Christopher Rose on amphibian metamorphosis and the one by Barry Sinervo and Erik Svensson on the origin of novel phenotypes, also provide excellent reviews, although they make little or no attempt to tie directly into Matsuda's ideas.
All told, the last two-thirds of the book constitute a nice review and an interesting look forward at a corner of the field of the evolution of development. Of particular note is West-Eberhard's chapter; in a little over five pages she very concisely and clearly summarizes her theory of genetic accommodation, a process that takes several hundred pages in her magnum opus (Developmental Plasticity and Evolution, Oxford University Press, 2003).
Overall, this book has merit for those interested in the narrow topic of the evolution of development and metamorphosis in vertebrates and insects. Don't get too discouraged by the first third of the book—it eventually redeems itself. For those interested in more synthetic works, I recommend Massimo Pigliucci's Phenotypic Plasticity: Beyond Nature and Nurture (Johns Hopkins University Press, 2001); West-Eberhard's Developmental Plasticity and Evolution; and my own book, coedited with Thomas Dewitt, Phenotypic Plasticity: Functional and Conceptual Approaches (Oxford University Press, 2004).
