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BOOK REVIEW

Development in the Real World

Marvalee Wake

ECOLOGICAL DEVELOPMENTAL BIOLOGY: Integrating Epigenetics, Medicine, and Evolution. Scott F. Gilbert and David Epel. xvi + 480 pp. Sinauer Associates, Inc., 2009. $49.95 paper.

The environment’s profound effect on animal phenotypesClick to Enlarge ImageWhat constitutes a new field in science? Must it be the consequence of a new synthesis? Does it need to take research in a new direction based on new ideas or new techniques? Or is it something that we recognize after the fact as a paradigm change? If we take these to be the criteria, then ecological developmental biology certainly qualifies as a new field, for it fulfills them all.

Anyone wanting to learn more about “eco devo” would do well to read Scott F. Gilbert and David Epel’s recent magnum opus, Ecological Developmental Biology: Integrating Epigenetics, Medicine, and Evolution. The same applies for those who may have been wondering what the currently emphasized “new biology” is all about. The new paradigm for biology in the 21st century is integration—of the various subfields of biology, and of biology with other fields, including physics, chemistry, geology, the social sciences and the humanities—and the goal is to understand the complexity of living systems and their dynamic nature. Several scientists interested in integration have been writing discourses on why it is important and how it can be facilitated. But Gilbert and Epel have chosen to leapfrog that discursive step to produce a compelling portrait of the new biology in action.

The authors have two goals for the book: to offer a “fresh and challenging way of looking at biology,” so that a different set of questions can be asked, and to show how ecological developmental biology is needed to diagnose and potentially help cure many of the problems of our planet. They emphasize four “revolutions” that are currently under way in biology: Inheritance has been shown to involve the transmission of gene expression patterns as well as gene nucleotide sequences; developmental and ecological explanations for human diseases are being found; phenotypic plasticity is being recognized as a “driving force” in the development and organization of biodiversity; and there is a new focus on analyzing relationships within networks of interaction. The book demonstrates that ecological developmental biology is significant in all four of these trends. Gilbert and Epel hope that by showing how to use the many facets of development to integrate disparate disciplines, the book will stimulate new research.

Of course, development in nature can differ in important ways from development in a controlled laboratory environment. Research on development in Drosophila and in mouse models, despite having been enormously productive, has not lent itself to a synthetic approach, because it takes place in laboratories, where the environment is considered constant and consequently unimportant. Integrating reductionistic laboratory research with experimental and observational research done in the field can be enlightening, and the book supplies a wealth of examples showing that many scientists have been doing just that.

The volume’s intended audience includes undergraduates (the authors maintain that a good first-year biology course should be adequate background) and graduate students as well as professional scientists—particularly biologists, who will want to know how their own areas of interest may be affected by the new biology. Gilbert and Epel, who are distinguished teachers, explain things clearly, supporting (and richly illustrating) their points with many photos, drawings, graphs and sidebars. These draw on the literature about a wide variety of diverse species, so that general principles emerge as the reader sees how ecology guides development in plants and invertebrates as well as vertebrates. Every chapter ends with a useful summary and valuable references.

The book is organized so that the flow of information builds the case for ecological developmental biology as a field of study. Part 1 deals with the ways that animals integrate signals from the environment into their normal developmental paths. The first chapter gives numerous examples of environmental factors (such as temperature, diet, crowding or the presence of predators) that elicit a particular phenotype. In many species of turtles and crocodiles, for example, the temperature at which an embryo develops determines whether it becomes male or female. Chapter 2 examines the mechanisms by which environmental cues bring about such changes on a molecular level; changes in gene expression brought about by DNA methylation, transcription-factor activation and neuroendocrine regulation are described. Chapter 3 is about developmental symbiosis, particularly between animals and the microbes they host. Bacteria of the genus Wolbachia, for example, are important to the sexual development of many arthropods. And in mammals certain gut bacteria are necessary for the formation of capillary networks in the small intestine. Chapter 4 describes the defenses that embryos have at their disposal to ensure their survival and normal development; many of these operate at a cellular level and include ABC transporter proteins, thiol-containing compounds, and enzymes.

Part 2 deals with the ways in which development can be altered to produce abnormal phenotypes, including what we call disease. Chapter 5, on teratogenesis, looks at environmental agents that disrupt development, such as industrial mercury, ethanol, retinoic acid, cigarette smoke, alkaloids and ionizing radiation. Endocrine disruptors, covered in chapter 6, are also teratogens, but they affect physiological function as well as anatomy. DDT, diethylstilbestrol (DES), soy estrogens, atrazine, bisphenol A (BPA) and polychlorinated biphenyls (PCBs) are all discussed, along with regulatory and policy decisions concerning them. Chapter 7 discusses many instances of adult diseases that result from altered gene expression, usually brought about by inappropriate methylation of DNA. (Methylation can stop a gene from functioning, just as mutation can.) For example, methylation of tumor-suppressor genes and demethylation of oncogenes may be the culprits in tumor cell formation.

Part 3 opens with a chapter on the history of evolutionary theory from classical Darwinism to the Modern Synthesis. Gilbert and Epel note that the Modern Synthesis demonstrated four things: that evolution within a species can be modeled mathematically; that genes under selection are the units whose frequencies change under Darwinian selection; that organisms with genes allowing them to become fit will produce offspring that are more fit; and that these offspring have a high likelihood of inheriting the genes that made their parents fit. The last two chapters bring development and developmental plasticity into a new synthesis, which applies to evolution both within and above the species level and emphasizes types of genes and variation in gene expression throughout life. Chapter 9, on evolution through developmental regulatory genes, discusses the origins of evo-devo (evolutionary developmental biology), “toolkit genes,” developmental modularity, and developmental genetic sources of variation (including changes in the place or time of gene expression or in the amount of protein produced, as well as changes in the properties of the protein synthesized). In chapter 10 the authors note that the Modern Synthesis, which is more than 50 years old, is in need of a major overhaul, particularly because ecological developmental biology has called into question some of its important assumptions. For example, evolutionarily significant variation is not always the product of genetic variation in alleles, as the Modern Synthesis would have it; some of it is instead the result of epigenetic variation, as when altered chromatin configurations act like alleles. Epigenesis—the production of phenotypes through environmental mediation of gene expression patterns—is a theme throughout the book.

Ecological Developmental Biology is filled with concrete examples that illuminate the basic science of topics ranging from interactive gene networks and biochemical pathways to interactions in ecological communities. The authors deftly summarize scientific findings that exemplify the points they want to make. The “cases” discussed usually deal with several levels of the hierarchy of biological organization, integrating molecular, organismal and ecological parameters in a fashion that enhances our understanding of development and evolution. Some cases show the ways in which “normalcy” is maintained or disrupted, and the authors discuss the developmental, ecological and medical implications of the disruptions.

Technique for revealing methylation differences and similaritiesClick to Enlarge ImageThe sort of integration I’m referring to occurs on many levels and across chapters. In chapter two, Gilbert and Epel examine transgenerational polyphenism in locusts; transgenerational predator-induced polyphenisms in radishes, Daphnia (a water flea), aphids and birds; and transgenerational polyphenisms induced by DNA-methylation differences in the toadflax plant and in mice and rats, showing the mechanisms by which polyphenisms can be transmitted across generations. In chapter 6, the authors discuss the transgenerational effects of endocrine disruptors in humans and frogs, and in chapter 7 they consider epigenetic methylation, disease and aging in humans. We learn about gene methylation and the fetal phenotype, cancer as caused by epigenetic methylation, the reciprocity of epigenetic and genetic causation in cancer, the effects of environmental pollutants (most of them introduced by humans) on the molecular biology of genes and development, and the ways such pollutants disrupt normal development in plants, frogs and humans. Information about how development is affected by the health of the environment is interwoven throughout. And as we learn all this, we acquire new ways of thinking about pattern and process in evolution.

The book’s coda, “Philosophical Concerns Raised by Ecological Developmental Biology,” deserves to be widely read. In it the authors discuss many important implications of the integrated developmental perspective presented in the book, observing that it “abolishes any notion of a genetic determinism.” They note that because developmental symbioses are not exceptional cases but the norm, developing organisms can be said to be involved in “co-construction on a massive scale.” Consequently, they recommend taking a broader view of evolution, one that acknowledges interdependence, harmony and integration in nature and includes a cooperative model of evolution alongside the competitive model. Pedagogically, they call for an expansion of disciplinary boundaries and revision of the metaphors used to describe evolution. “Storytelling matters,” they conclude.

Evolutionary narratives are the most critical stories in biology, in science, and perhaps in Western civilization, so we had better get them in line with the biological data.

In the final paragraph of the coda, reminding the reader that “the rules of the evolutionary process include the crucial notion of ‘becoming with,’” Gilbert and Epel emphasize that “co-development is normative, and evolution is not merely the battle of each against all.” They have demonstrated that an integrative approach that encompasses interactions at all levels (from molecules to ecosystems) is essential.

Four succinct but deliciously rich and provocative essays serve as appendices. The first and third offer historical perspectives and analyze the contributions of some major figures (Trofim Lysenko, Paul Kammerer, Richard Goldschmidt, C. H. Waddington); the second and fourth clarify epigenetic effects.

Gilbert and Epel have produced a book that is enormously thoughtful on a number of levels. I marvel at their capacity to integrate so much information and so many ideas lucidly, succinctly and engagingly. Part of their intention is to develop a new emphasis on integration across the hierarchy of biological organization, and the excellent and diverse examples of integration that they present show how promising the approach is. I expect that their focus on examining the ways that development at all levels responds to and shapes environments will prove increasingly fertile as it matures, yielding new insights, new approaches, new techniques and new theory. I urge biologists who relish the challenge of new ideas to read this book with care, to use it in courses and seminars, and to discuss with colleagues how to collectively participate in the new biology. Gilbert and Epel have given us a magnificent road map to the healthy future of biology and of life.

Marvalee H. Wake is Professor of the Graduate School in the Department of Integrative Biology at the University of California, Berkeley. Her research interests include evolutionary morphology, development and reproductive biology in vertebrates.


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