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1 September 2008 A Grand Conversation on Evolutionary Genomics
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Genomics is, by its nature, a discovery-based discipline. Like the Lewis and Clark expedition or the voyage of the Beagle, large-scale genome projects are exploratory journeys into the molecular wilderness, each trip yielding new and sometimes surprising findings. After each journey, data are catalogued, compared with the results of earlier explorations, and archived in large databases. Findings are often compared with broad expectations rather than used to test discrete experimental hypotheses. Nevertheless, as genomic data from different species become more plentiful and the tools more accessible and inexpensive, genomic approaches are increasingly being employed to address long-standing questions in evolutionary biology. For example, what have been the relative roles of selection and neutral processes in shaping the origins and diversification of taxa? What are the changes in gene sequences and gene expression that underlie changes in phenotype?

Enough data are at last becoming available on genome evolution to warrant book-length treatments of the field. Michael Lynch weighed in last year with a population genetics–oriented volume (The Origins of Genome Architecture, Sinauer, 2007). Now, Mark Pagel (University of Reading, United Kingdom) and Andrew Pomiankowski (University College London) have assembled a diverse international set of experts in both molecular and evolutionary aspects of genome science to produce Evolutionary Genomics and Proteomics. The 13 chapters address research on a broad spectrum of evolutionary genomics topics, including evolution of genome organization and complexity, origins of new genes and protein domains, genome robustness and redundancy, and the relationships between genomic and phenotypic diversity.

Pagel and Pomiankowski's stated rationale for an edited volume is that evolutionary genomics research draws upon a diverse array of specialized areas of expertise. It can be difficult, however, for an edited book to achieve the focus needed to capture the emergent properties of such an eclectic discipline. In my experience, volumes like this one often do more to showcase the research interests and agendas of the individual contributors than to present a cohesive treatment of their topics. Evolutionary Genomics and Proteomics does not present a particularly concise examination of the field, as the chapter topics overlap extensively and nearly every subject is expounded upon by multiple contributors. Nevertheless, thanks to the range of expertise and perspectives among the authors, this overlap provides useful complementary perspectives on the topics rather than repetition. The resulting tone is that of a grand conversation among the contributors, with the reader given the opportunity to view the field as a whole through the give-and-take of the various chapters. The order of the chapters seems largely haphazard, but this arrangement actually enhances this sense of conversation, whether or not it was the editors' intent. Thus, it seems to me that Pagel and Pomiankowski have succeeded in achieving the broader synthesis they desired.

A central issue throughout the book is deciphering the relative importance of selective versus neutral processes in explaining different aspects of genome and proteome evolution. Evaluating evidence of selection at the DNA sequence and network levels, respectively, are the main themes of chapters by Alan Filipski and coauthors and by Andreas Wagner, but this theme arises in some form in nearly every chapter. In their introductory chapter, Pagel and Pomiankowski put a distinctly selectionist spin on this topic and dismiss, without elaboration, Lynch's arguments that neutral mechanisms are sufficient to explain many genomic phenomena. Fortunately, the authors of the individual chapters seem much more interested in trying to understand the evolutionary processes responsible for genome evolution than in debating perspectives on their relative importance. Not surprisingly, the contributors differ in the rigor with which they discuss tests for selection and evaluate their potential shortcomings. Nearly every chapter, however, emphasizes the uncertainty that persists about evolutionary mechanisms and the amount of research that remains to be done.

A second major theme involves what might be considered the holy grail of evolutionary genomics: the mapping of genomic and other “-omic” variation onto phenotypes to explain the integrated functional basis of phenotypic diversity. The nascent field of systems biology seeks to accomplish genome-to-phenotype mapping by developing predictive models, then iteratively testing and refining these models using genomic, transcriptional, proteomic, and metabolomic data. A chapter early in the book by Eugene Koonin and Yuri Wolf introduces systems biology in the context of understanding phenotypic evolution, and sums up recent insights on the factors linking variables describing genome function (e.g., protein abundance, gene dispensability, and number of protein interactions) and genome evolution (e.g., evolutionary rate, number of paralogs, and likelihood of gene loss). Later chapters by Bernardo Lemos and coauthors, László Patthy, Laurence Hurst and Csaba Pál, and Andreas Wagner build on the systems biology theme by discussing research on the inheritance of variation in transcriptional networks, organization and scaling of protein interaction networks, genomic redundancy, and gene network evolution.

The chapters by Hurst and Pál on genomic redundancy and dispensability and by Wagner on whether a “network biology” exists were for me the twin high points of the book. Assertions that some genes are redundant or dispensable, and proposed explanations for redundancy, have long struck me as dubious, and Hurst and Pál provide a particularly insightful examination of the data on this topic. Wagner examines whether the organization of biological networks is fundamentally different from that of nonbiological networks because of natural selection, concluding that there is convincing evidence for effects of selection on local small-scale features, but not, at least so far, for global network structure.

One omission from Evolutionary Genomics and Proteomics that I found disappointing was the lack of discussion on how understanding genome evolution might affect society. At the end of their introductory chapter, Pagel and Pomiankowski state offhandedly that the success of the field will be measured in part by success in creating made-to-order phenotypes, a prospect I find to be at once exciting and disturbing. On the one hand, understanding the adaptive significance of genome evolution may provide important insights for controlling infectious diseases and developing more productive but less resource-demanding crop varieties. On the other, such knowledge has unprecedented potential for disastrous misuse by malicious or merely naïve practitioners. These issues deserve more than trite anticipation.

In spite of such shortcomings, Pagel and Pomiankowski have produced a volume that will benefit readers ranging from graduate students to seasoned researchers in both evolutionary and functional areas of biology who seek an understanding of this rapidly developing field. The technical language and themes, however, will put the book beyond the grasp of all but the most astute nonscientists. Much of the detail in this book will undoubtedly become dated rather quickly, given the rate at which advances are occurring. Even so, the complex questions being addressed by evolutionary genomics research will not yield quickly to definitive answers, so the broader questions addressed in the book's chapters will remain relevant for a long time to come.

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and David L. Remington "A Grand Conversation on Evolutionary Genomics," BioScience 58(8), (1 September 2008). https://doi.org/10.1641/B580813
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