Viruses and the Evolution of Life. Luis P. Villarreal. ASM Press, Washington, DC, 2005. 395 pp., illus. $120.00 (ISBN 1555813097 cloth).

Are viruses alive or not? This question has plagued microbiologists since the discovery of viruses in the 1890s. Bereft of an innate metabolism, viruses may be viewed merely as chemical replication systems. But this would be a gross oversimplification, for viruses, like their cellular hosts, are at the mercy of Darwinian selection: they evolve. And it takes no great stretch of the imagination to see that viruses play some role in the ongoing evolution of their hosts. With powerful molecular tools at our disposal (many of them derived from viruses of bacteria), scientists have discovered an increasing number of genetic curiosities. Virus genes may be expressed by the host to increase host fitness, as is the case with Vibrio cholerae and its virus CTX phi (Waldor and Mekalanos 1996); host genes may be carried by a virus to increase its replication efficacy in a dying host, as is the case with some viruses of Prochlorococcus species that carry fully functional photosynthesis genes (Lindell et al. 2004). Given a mounting body of such evidence, “it is time to acknowledge and study the roles of viruses in the web of life, be they living or not.” Such is the powerful opening argument of Luis Villarreal's new book, Viruses and the Evolution of Life.

This book provides a smorgasbord of food for thought for senior graduate students, professors, and researchers already engaged in the field of virology or phage biology. Villarreal assumes a lot regarding the viral savviness of his readers, so I would not recommend this text to anyone lacking a solid background in viruses. From the beginning, Villarreal establishes two ambitious goals: to examine the evolution of viruses from the perspective of the evolution of their hosts, and to consider the importance of persistent viruses in the evolution of life on Earth. He begins strongly, delineating a brief history of viruses, identifying broad patterns of virus–host evolution, and providing a clear definition of what he considers a virus: a molecular genetic parasite. This leaves the term “virus” open enough to include virus-like elements such as endogenous retroviruses and transposons, which figure heavily in Villarreal's arguments. Drawing on computer models, he argues for the likely early emergence of parasites (viruses) in informational systems, leaving the vast majority of evolutionary time open to viral influence. These models provide a clear illustration of how informational systems, biological or otherwise, cannot escape parasitization, and how this very parasitization is what drives increases in system complexity. A small problem I encountered with this argument is that throughout the text, evolution is equated with higher complexity; however, complexity is never adequately defined. Thus the reader is left to decide whether complexity pertains to genome size, to the number of organ systems, to the degree of homology to Homo sapiens, or to some other set of criteria.

This point aside, the book fulfills its goal of providing an overview of known virus–host interactions for most of the life-forms on the planet. Villarreal supplies a wealth of information on the relationships between virus and host, from prokaryotes to placental mammals, exploring the impacts and evolutionary implications of such interactions. Each chapter contains a thorough list of recommended reading and source material, enabling the reader to gain additional background or finer detail as needed.

The material on prokaryotes is particularly strong because of the comparative abundance of information on prokaryotic viruses, primarily bacteriophages. Villarreal provides a clear comparison of acute versus persistent replication routes, as well as their potential impacts on host fitness and evolution. He introduces significant examples of how viral survival mechanisms may affect prokaryotic evolution, such as addiction modules, which ensure stable and persistent incorporation of viral genomes within the host, and the replacement of host genes or genetic motifs (e.g., the origin of replication) with viral homologues.

Likewise, Villarreal provides especially coherent arguments for the role of endogenous retroviruses in the speciation of mammals and in mammalian features such as placental development and live birth. As a member of the Department of Molecular Biology and Biochemistry at University of California, Irvine, Villar-real has an established publication record exploring the effect of viruses on their mammalian hosts, particularly on the mammalian immune system and reproductive processes. Thus, when it comes to explaining how viruses could possibly play a role in the ability of placentals to carry an allogenic embryo internally without eliciting an immune response, Villarreal is in his element.

As this book led me through a menagerie of organisms and their multitude of viruses, I was presented with several new and fascinating examples of how viruses intervene in the evolutionary pathway of their hosts. One example is the linkage between sex and persistent viruses in protists. Because infected and uninfected partners cannot produce viable offspring, the population is segregated into two subpopulations that do not interbreed. The establishment of two such subpopulations is a key ingredient in the divergence of species, and this instance clearly shows how the process may be driven by viruses. Through arguments like this, Villarreal forces the reader to break out of the conventional disease and epidemiology mind-set and consider viruses in multiple contexts. In between prokaryotes and placentals, however, many of the arguments become weaker and more focused on single examples. Part of this is due to a dearth of information regarding viruses of other organisms, such as fungi, arthropods, crustaceans, and plants, especially compared with the volume of information available on virus–bacteria interactions. In Villareal's words, “viruses of [aquatic organisms other than bacteria] and their hosts present little apparent medical or agricultural risk; thus studies of them have generally not been well supported financially.”

Beyond this logistical limitation, however, I found another, more serious problem with Villarreal's treatment of the material. Although he does a fine job in examining the range of known virus–host relationships across the domains of life, Villarreal does not always clearly establish the evolutionary significance of these relationships, and thus falls short of the second goal of his book: to weigh the importance of viruses in the evolution of life. Much time is spent reviewing what is known about viruses and their relationships with their hosts. While this background is certainly informative and necessary to a degree, I gained the impression that in the course of such exposition, Villarreal lost sight of his goal to elucidate how and where viruses influenced host evolution. This is perhaps symptomatic of a more overarching problem: the scope of the text seems a bit overzealous. In climbing the evolutionary ladder across all life from bacteria to humans, there was simply too much information to be covered in adequate detail. The result is that the book, at times, devolves into a capitulation of known virus–host interactions, without a clear synthesis of new ideas linking these interactions to concrete evolutionary events.

In spite of these shortcomings, Villar-real does ultimately make the convincing point that virtually every species on the planet is infected by viruses. And given the immense span of evolutionary time available, these viruses have probably played some role in tweaking the genomes of their hosts. In the final analysis, I can't help but agree with Villarreal: although the picture is still incomplete, it is time we include viruses in our conceptions of the tree of life, be they living or not.