Books et al.Evolution

What Led to Metazoa's Big Bang?

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Science  07 Jun 2013:
Vol. 340, Issue 6137, pp. 1170-1171
DOI: 10.1126/science.1237431

The Ediacaran and Cambrian periods witnessed a phase of morphological innovation in animal evolution unrivaled in metazoan history, yet the proximate causes of this body plan revolution remain decidedly murky. The grand puzzle of the Cambrian explosion surely must rank as one of the most important outstanding mysteries in evolutionary biology. Evidence of early representatives of all the major animal phyla first appear abruptly in the Cambrian (starting 542 million years ago). This spectacular morphological diversity contrasts strongly with Precambrian deposits, which have yielded a sparse fossil record with small, morphologically ambiguous trace fossils or the enigmatic but elegant creatures of the Ediacaran fauna. Following the Cambrian, despite a rich fossil record that documents impressive morphological diversification among animals, no new body plans have been revealed, leaving the Cambrian as the apparent crucible of metazoan body plan innovation. Although it is only in the various Cambrian fossil assemblages that this exuberance of animal life first makes an appearance, molecular clock calculations estimate divergence times of the major metazoan lineages well before the Cambrian. That suggests a prolonged period of cryptic evolution in the Ediacaran not well represented in fossils, adding further intrigue to the puzzle.

Difficult to interpret.

Herpetogaster collinsi, a tentaculate soft-bodied fossil from the Burgess Shale, is a possible stem Ambulacraria.

CREDIT: QUADE PAUL/COURTESY ROBERTS AND COMPANY

The range of hypotheses proposed to explain the Cambrian explosion is as diverse and broad as the fossils they seek to explain. Researchers from a wide range of sciences (including geology, ecology, developmental biology, and genomics) have all made substantial contributions toward unraveling the causes of this key puzzle of animal evolution. Yet in most cases, their findings have been considered independent of one another. In The Cambrian Explosion, paleontologists Douglas Erwin (National Museum of Natural History) and James Valentine (University of California, Berkeley) make a heroic attempt to synthesize these disparate fields. In the process, they have distilled a unique contribution that should be a required addition to any biologist's bookshelf.

The book's first two sections set the stage. The authors introduce the geological and environmental contexts of the Cambrian and Ediacaran and then the animal phyla and fossils. They strip the characteristics of each phylum down to the basics, not burdening readers with too much detail but providing enough for them to appreciate how recent modifications to animal phylogeny have strongly revised our understanding of early animal diversification. This section is well illustrated with clear and simple diagrams. I found the fossil chapters particularly compelling, as they brought together key Ediacaran and Cambrian fossils, discussed within the framework of contemporary hypotheses of animal relationships. Quade Paul's vivid color reconstructions, displayed next to photos of the fossils, bring to life the stunning morphological diversity and ecological context that are often lost in the rather clinical descriptions of these mysterious fossils from the primary literature.

The authors also review molecular biology's substantial contributions to solving the grand puzzle of the Cambrian explosion, which have at times been at odds with interpretations derived from fossil data. Comparative developmental genetic studies and genome sequencing projects from diverse metazoan phyla have revealed some of the genetic innovations that were likely responsible, in part, for the increase in animal complexity. These new data may help us reconstruct ancestral morphological features of the mysterious stem lineages of the Ediacaran, by reconstructing ancestral gene complements and by inferring gene regulatory networks that have key roles in setting up the body plans of extant animals. However, our understanding of how to relate genomic and developmental regulatory complexity to organizational and morphological complexity remains in its infancy.

In the book's last section, Erwin and Valentine begin to integrate and synthesize the introductory material. They hold that many previous attempts at developing hypotheses to explain the Cambrian explosion focused on a single cause, which was often inconsistent with data available from other fields. They argue convincingly that complete understandings of animal origins and the explosion's "great evolutionary puzzle" can only be achieved by considering the relative importance of three main aspects: substantial change in the environment, which differed greatly from the present day; the sequential acquisition of genetic and developmental innovations that gradually increased body plan complexity during the Ediacaran and Cambrian; and the establishment of ecological relationships among animals that ensured that new metazoans with novel body plans succeeded in their new environments. Ecological opportunities for novel morphological innovations were not just provided by physical changes to the environment but also driven by changes produced by the activities of animals themselves.

Readers of The Cambrian Explosion will likely have either little background or some expertise in one of the disciplines covered. Falling into the latter camp, I have largely considered causes of the Cambrian explosion from the perspective of molecular genetics and genomics. Erwin and Valentine illuminate clear links between seemingly disparate disciplines, and they make a compelling case that substantial progress toward understanding the origins of animal diversity will not be achieved through adding isolated gains in individual fields. It is futile to hope to explain such a major evolutionary event without embracing an interdisciplinary approach.

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