Endless Forms Most Beautiful: The New Science of Evo Devo and the Making of the Animal Kingdom. Sean B. Carroll. W. W. Norton, New York, 2005. 350 pp., illus. $25.95 (ISBN 0393060160 cloth).

This book is unique in that it is the first in the field to be written at a level and in a style that students, K–12 teachers, and the general public, as well as researchers, will enjoy and understand. Catchy chapter titles (e.g., “Making Babies: 25,000 Genes, Some Assembly Required” ; “The Dark Matter of the Genome: Operation Instructions for the Tool Kit”) entice the reader, and clever analogies enable Carroll to progressively build a logical understanding of what may be new concepts (e.g., the developmental genetics of gene regulation). Researchers and graduate students, particularly in fields peripheral to evolutionary developmental biology, or evo devo, will also find that this book broadens and deepens their perspective on the field.

Although a number of other evo devo books have been published in the past several years (Arthur 2000, Davidson 2002, Wilkins 2002, Minelli 2003), the refreshingly noncomprehensive format of this book (from the standpoint of the field's history and of the increasing volume of examples) makes it a delightful read. It is well illustrated with gorgeous color plates of gene expression patterns and butterfly wings, and black-and-white drawings and photographs, among which are phylogenies, body plans, monstrosities, and gene switches and networks.

For the title of the book, Carroll chose Endless Forms Most Beautiful, the only four words of the last sentence of Darwin's Origin of Species that remained completely untouched throughout the many versions and editions of that classic. The diversity and beauty of the organisms is captivating, and Carroll uses readers' natural fascination to lead us through the stories coming from the field of evo devo.

Carroll argues that it is from the form-based perspective of evo devo that evolutionary principles can be compellingly taught. “The evolution of form is the main drama of life's story, both as found in the fossil record and in the diversity of living species,” he writes. “So, let's teach that story. Instead of ‘change in gene frequencies,’ let's try ‘evolution of form is change in development’” (p. 294). Evo devo's methods of illustrating how animal forms evolve, he argues, offer a much more powerful explanatory vision than the abstract extrapolations of the era of the modern evolutionary synthesis. As Carroll points out, most students can conceptualize (a) the small leap from understanding the building of complexity in one generation from egg to adult, to appreciating how modifications of development over greater evolutionary time have produced a diversity of forms; (b) the molecular genetic details of developmental control (tool kit genes are shared by all animals, and differences in form come from changing the way they are used); and (c) the visually appealing nature of the evo devo perspective. By focusing on the drama of the evolution of form and illustrating how changes in development and genes are the basis of evolution, the evo devo approach allows the deep principles underlying the unity and diversity of life to emerge.

Evolutionary changes in development ultimately occur at the level of the genome, and with analogies to astronomy in chapter 5—“Just as dark matter in the universe governs the behavior of visible bodies, the dark matter in our DNA controls where and when genes are used in development” (p. 110)—the author gets into the meat of gene regulation: the operating instructions for the tool kit. He compares the instructions embedded in the dark DNA to “genetic switches” (p. 111) and points out that the anatomy of animal bodies is encoded and built by constellations of switches distributed all over the genome. Carroll anticipates that the facts of gene regulation will be unknown, intimidating, and difficult for many readers, and he does an admirable job of breaking them down into their logical components. For example, the length of a switch is several hundred base pairs; each switch contains 12 to 20 signature sequences to which other proteins bind; multiple switches control each tool kit gene; and sets of interconnected switches and proteins form local circuits that are part of larger networks. The general function of switches is to transform the existing pattern of gene activity into a new pattern of gene activity, and ultimately animal body plans are the product of this dynamic regulatory architecture.

The flavor of Carroll's prose is captured in his description of gene regulation:“The making of an animal involves one more set of genetic invisibles—little devices in the DNA that govern where and when genes are activated.… I will describe the fantastic little devices in the genome that draw the beautiful patterns of gene expression…and that are the key links between the chains of tool kit genes that build animal complexity and diversity” (p. 107). He explains that it is the modification of switches over evolutionary time that has resulted in the spots, stripes, and bumps of Kipling's Just So Stories: “Differences in form arise from evolutionary changes in where and when genes are used, especially those genes that affect the number, shape, or size of a structure” (p. 11). This solid understanding of gene regulation is necessary for understanding the effects of environment on development (mediated through genetic switches; chapter 8), as well as modularity and combinatorial gene logic (chapters 5–11).

Although modularity—the idea that an organism is composed of discrete parts that are built by integrated developmental networks—might be intuitive at the anatomical level, the modularity of the genetic switches underlying it is under-appreciated. Modular switches are used for building modular animals, and therein lies the critical connection to evolution: switches allow evolutionary change to occur in one part of a structure, independent of other parts. Switches are the secret to modularity, and modularity is the key to building complexity. The key to making endless forms (illustrated with arthropods and vertebrates) is in the astronomical number of possible combinations of regulatory inputs and switches. The “Big Bang” (Cambrian explosion; chapter 6) and the “Little Bangs” (subsequent diversification; chapter 7) of animal evolution are stories of the evolution of different numbers and kinds of repeated body parts due to shifting of Hox zones (ultimately caused by changes in DNA sequences of Hox gene switches).

Carroll attributes the unexpected nature of the discoveries in evo devo to the field's revolutionary character. As he notes in the introduction,“Contrary to the expectations of any biologist, most of the genes first identified as governing major aspects of fruit fly body organization were found to have exact counterparts that function similarly in most animals, including ourselves” (emphasis in original). Before the emergence of evolutionary developmental biology, nothing was known about how genes affect form, which genes affect the evolution of form, or what kinds of changes in genes were responsible for evolution.

The author uses helpful metaphors of mapping and geography to explain the progression of gene expression and action in development. Maps of gene expression and development reveal the order and logic of how tool kit genes work progressively to construct complex animals from a simple egg. The expression patterns of tool kit genes are related to the dynamic map of development in terms of, for example, longitudes, latitudes, and the East–West axis.

Endless Forms Most Beautiful could be used as a supplement to a textbook in general courses in developmental biology, animal diversity, and evolution, as it engagingly explains how the forms of individual species develop, how so many different forms have evolved, and how the various patterns and trends in animal design have arisen. Readers need not be expert in the field, however. Most general readers will want to know why evo devo is relevant to them, and the question “Why should I get excited about a fruit fly?” is answered for many at the end of the book: “because the same old genes were taught some new tricks” in human evolution.

Carroll deserves credit for tackling human evolution (chapter 10). In fact, the logic of the first chapters sets the stage so solidly that the key concept—“there is no need to invoke single dramatic mutations as causes of great leaps in form and function or as explanation for the origins of human traits” (p. 377)—should be easy to accept. By the end of the book, readers will be knowledgeable enough to appreciate the “the grandeur of the evolutionary view of life.” The fundamental lessons of evo devo about modularity, genetic switches, and the evolution of form are well taught; Kipling would be riveted.