American Scientist

On the Origin of Phyla. James W. Valentine. xxiv + 614 pp. University of Chicago Press, 2004. $55.

The recent surge in interest in the origins of multicellular animals (metazoans) is fueled by new evidence from three major sources: molecular sequencing, the study of evolutionary development and the discovery of exceptionally preserved fossils of Precambrian and Cambrian age, particularly from China. Genetic sequences provide a means of analyzing how the major animal groups are related and of estimating their time of origin (using the molecular clock)—a means that is independent of morphological data and the record of evolutionary events the fossils reveal. The study of developmental processes in an evolutionary framework ("evo-devo") provides the link between genetics and morphology. These new approaches have prompted molecular biologists to join forces with paleontologists to focus on the sequence of events leading to the origin of body plans before and during the Cambrian Period (543 to 500 million years ago).

Few if any authors can embrace these fields with the experience and authority of James W. Valentine, professor emeritus of integrative biology at the University of California, Berkeley, who has been publishing novel and provocative ideas on the origin and nature of phyla for more than 30 years. His most recent book, On the Origin of Phyla, is an homage to the greatest biologist who ever lived by one of the greatest living paleobiologists.

The concept of a phylum is not straightforward. A phylum has been characterized as a group of species that share a unique body plan or organization that reveals no evidence of relationship to other phyla. This definition may be relatively easy to apply to living animals but often proves problematic for extinct ones. Phyla originated hundreds of millions of years ago, and extinction has weeded out intermediate forms, leaving significant differences between the living phyla. There is no difficulty, for example, in distinguishing between an arthropod (say, a spider), an echinoderm (a starfish, for example) and a chordate (such as your department chairperson). Fossils, however, particularly those of the Paleozoic Era (from 543 to 251 million years ago), may be more difficult to deal with. Their morphology may be unfamiliar, and there is the problem that information on the soft tissues has usually been lost through decay and is not preserved.

On the Origin of Phyla is essentially about the Cambrian radiation, the event that gave rise to most of the major animal groups. The book's particular strength is its integration of data from paleontology and biology.

Stephen Jay Gould's major treatment of the Cambrian radiation, Wonderful Life (1989), was based mainly on the famous fossils of the Burgess Shale. Gould considered many of the Burgess Shale animals to represent extinct phyla or body plans, and he argued that their large number was a measure of the impact of the Cambrian explosion. Just 15 years later, Valentine's book demonstrates that there has been a sea change in the focus on phyla, from considering them as a measure of separation to exploring relationships between them—something that is impossible to do, almost by definition, on the basis of morphological data, but has become a realistic goal in the age of molecular sequencing. Fossils, however, remain central—if we want to understand the early evolution of phyla, we need the evidence provided by fossils from the Neoproterozoic Era (from 1 billion to 543 million years ago) and the Cambrian Period.

A simple question exposes a problem in dealing with the origin of phyla. The earliest members of a lineage have yet to acquire the diagnostic features of the defining body plan. To which phylum do they belong? Cladistics (a method of analyzing relationships among taxa based on homologous characters) allows an emphasis to be placed on the living members of a phylum: The "crown group" (the last common ancestor of all living members of the phylum and all the descendants of that ancestor) can be distinguished from the "stem group" (the rest of the clade, a series of extinct organisms lying "below" the crown group). Molecular data are available to determine crown-group relationships, but of course no such data will ever exist for the stem—which is a pity, because, as Valentine points out, "stem taxa should provide more evidence of the ancestral features of a phylum than do the crown taxa." Stem taxa can be assigned to a phylum once they evolve the diagnostic characters, and we can date the appearance of phyla based on fossils.

On the Origin of Phyla is divided into three parts, the first two of which provide a basis for the shorter third section. Part One, "Evidence of the Origins of Metazoan Phyla," discusses the nature of a phylum and the history of the concept, which originated as a strategy for classifying organisms. A discussion of body plans explains how their development is controlled by the genome, and this account leads naturally to a description of methods, both morphological and molecular, for determining connections between different phyla. Of course, the relationships of fossil taxa can be analyzed only on the basis of morphology. For living phyla, molecular data provide an independent key to their relationships, and the morphological and molecular data can be combined. The fossil record and the molecular clock also provide evidence of timing, but they date different phenomena: The molecular clock records the splitting of lineages, whereas fossils date the appearance of body plans. Neither method is particularly precise, but with more new discoveries the two have become better reconciled.

A chapter on the nature of the fossil record is important for readers less familiar with the evidence of paleontology. Incomplete information is a particular problem during the early stages of the diversification of metazoan phyla. The most controversial evidence is provided by the extraordinary organisms of the Ediacaran Period (600 to 543 million years ago) of the late Neoproterozoic Era. Valentine discusses them with the metazoan phyla, as "prebilaterians" (organisms coming before those with bilateral symmetry) and earliest crown bilaterians, whereas others argue that at least some of them are not metazoans at all. Valentine believes that the Ediacaran animals likely lie between the sponges and crown diploblasts and suggests that the remarkable fractal morphology displayed by some Ediacaran organisms might reflect development controlled by Hox-type gene clusters.

But the preservation of the Ediacaran fauna with their intriguing soft parts is the exception. Before grazing invertebrates were widespread, microbial mats could colonize the sediment surface, creating conditions that favored very early mineralization of the adjacent sediment, preserving the morphology of soft tissues like a death mask. These conditions disappeared with the Cambrian radiation, so it is not surprising that a number of the small soft-bodied phyla living now are unknown as fossils. As Valentine notes, "there is nothing in the fossil record to disprove the hypothesis that all phyla had appeared by the end of the Cambrian or, for that matter, the end of the Early Cambrian."

Valentine styles Part Two, "The Metazoan Phyla," as "the march through the phyla." He deals with the prebilaterians, sponges, cnidaria and ctenophores and then with the nature of the earliest crown bilaterians. The treatment is ordered based on the molecular Tree of Life, dividing the protostomes into Ecdysozoa and Lophotrochozoa, and completing the section with the Deuterostomes. This is a comprehensive, up-to-date survey, reviewing each phylum under four major headings: body plan, development, fossil record and relationships to other phyla. Here, as elsewhere in the book, the illustrations are collected from a huge variety of original sources. The styles were selected to ensure some compatibility, but the figures have not been redrawn. Although the content of the book is distinctive, the design is not, but this survey of phyla was not written primarily with undergraduates in mind!

Valentine's unique voice is particularly evident in Part Three, "Evolution of the Phyla." Here he treats patterns of diversity through the Phanerozoic (the 543-million-year span for which evidence of life in the fossil record is abundant), distinguishing between taxonomic diversity and the evolution of morphology. He argues that bilaterian body plans originated and radiated on the seabed rather than floating or swimming in water and that we should seek the fossil evidence among bottom-dwelling forms. The lack of a good record of soft-bodied animals in the Neoproterozoic (Ediacaran examples notwithstanding), prior to the widespread evolution of mineralized tissues ("hard parts" to paleontologists), limits our ability to reconstruct both the prelude to and the main events of the Cambrian explosion. Valentine emphasizes that evolution proceeds from the top down, with body plans appearing early, to be followed by diversification within these themes. This, of course, is why the Neoproterozoic and Cambrian record is so important.

On the Origin of Phyla concludes with a discussion of why a resolution of metazoan relationships is so difficult. "For nearly every facet of early metazoan history there is an array of hypotheses that cannot be definitively falsified by the available data," Valentine says. The solution then lies in more research—more fossil discoveries, a better understanding of the evolutionary development of the major groups, more molecular sequences. But, as he points out, there are some gaps in the database that can never be filled. The earliest members of the phyla (stem representatives) became extinct long ago, and thus there is no hope we'll ever have their genetic sequences to ponder. Yet phosphatized embryos from the Neoproterozoic, like those from the Doushantuo Formation of Guizhou, China, which are dated at about 570 million years ago, offer the possibility of a glimpse into Precambrian embryology, one that could complement evidence on the evolutionary development of living organisms.

In the absence of direct evidence of the sequence of changes that gave rise to individual phyla, our best bet, as Valentine observes, is to unravel those "first principles of genome evolution that constrain the evolutionary routes between the developmental systems that can actually be studied"—that is, those within living taxa. The problem is one of a complexity of processes compounded by gaps in the evidence: "in place of Darwin's tangled bank, we find a Cambrian seafloor."

But progress has been astonishing, and much remains to be tackled. As Valentine emphasizes, "at least in interpreting the past we are far better off than in forecasting the future." On the Origin of Phyla is a remarkable achievement, a timely synthesis of the current state of this exciting field, which provides a marker against which future progress will be measured.