Journal of Heredity Advance Access originally published online on August 28, 2007
Journal of Heredity 2007 98(6):633-634; doi:10.1093/jhered/esm073
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Book Review |
The Origins of Genome Architecture
The Origins of Genome ArchitectureMichael Lynch
Sinauer Associates, Inc. Publishers. Sunderland, MA. 2007. Hardcover, 494 pp. $59.95. ISBN 978-0-87893-484-3.
In the mid-nineteenth century, Charles Darwin was the first to identify natural selection as the mechanism of adaptive evolution. Although his observations described how the population evolves, there was no accurate model describing the mechanisms responsible for the origin of variation and its inheritance. In late 1960s and early 1970s, Kimura (1986) proposed the neutral theory of molecular evolution that attributed an important role to the genetic drift of neutral mutations. The debate between 2 theories is summarized by words of Lewin (1996):
To selectionists (natural selection) most mutations are either beneficial or harmful; beneficial ones are retained in the population, creating extensive variation, while harmful ones are removed. To neutralists (neutral theory), most mutations are adaptively neutral, and therefore become fixed in the population because their presence posses no harm; extensive variation is the results.
The neutral theory does not deny the role of natural selection as Motoo Kimura stated in 1986. Michael Lynch, in his new book, cited that
Many aspects of the evolutionary change are indeed facilitated by natural selection, but all populations are influenced by the nonadaptive forces of mutation, recombination, and random genetic drift. These additional forces are not simple embellishments around primary axis of selection, but are quit the opposite—they dictate what natural selection can and cannot do.
Michael Lynch describes evolution as a population-genetic process governed by 4 forces, where the natural selection is the adaptive force, mutation is the ultimate source of variation on which natural selection acts, recombination assorts variation within and among chromosomes, and genetic drift ensures that gene frequencies will deviate a bit from generation to generation independent of other forces (Lynch 2007). In the same article, Lynch stated that
If complexity, modularity, evolveability, and/or robustness are entirely products of adaptive processes, then where is the evidence? What are the expected patterns of evolution of such properties in the absence of selection, and what types of observations would be acceptable as a falsification of a null, nonadaptive hypothesis?
The recent advances in genomics such as whole genome sequencing, high throughput proteomics, and bioinformatics led to a dramatic development in the molecular evolution field. With these advances, and in an attempt to answer the previous questions, this book discusses the origin of eukaryotic gene structure and how the nonadaptive processes initiated genome-wide repattering of eukaryotic genes structure; these primary processes provided novel substrates for the natural selection as secondary processes to raise new phenotypic complexities. This hypothesis was a topic of several articles (Lynch and Conery 2003, 2004; Lynch 2006, 2007; Lynch et al. 2006; Paland and Lynch 2006). Lynch's hypothesis met some opposing comments (Daubin and Moran 2004; Vinogradov 2004). Lynch and Conery (2003) cited that with this hypothesis, arguments based on molecular, cellular, and/or physiological constraints are insufficient to explain the disparities in gene, genome, and phenotypic complexity between prokaryotes and eukaryotes.
In 13 chapters, the book is expounding the hypothesis in details. Each chapter starts with an introduction that paves the way for the discussion. Four introductory chapters lay the groundwork for the book's hypothesis. The main idea for these chapters is the emergence of eukaryotic gene structure, which the author presented in considerable detail in an article in Molecular Biology and Evolution (2006). In chapter 1 the author, with help of the phylogenetic models, tried to answer many questions such as how a DNA-based genome evolved from an RNA world, what is the similarity between prokaryotes and eukaryotes, and are the 2 functional groups of cellular life arise from/and share the same ancestor. At the end of this chapter (page 26), a 4-steps scenario summarizes the evolution during the first 2 billion years of life. Chapter 2 is devoted to explore the relation between genome size and organism complexity. In chapter 4, the author discusses the effect of population size on the mutation rate and how the evolution can occur within species depending on their population size. Based on this concept, Lynch concluded that prokaryotes followed by unicellular eukaryotes need bigger population sizes than multicellular eukaryotes to evolve. The factors that control those transitions are decreasing population size, decreasing recombination, and increasing deleterious mutations. The relation among genome size, complexity, and population size met some arguments that argue the supportive examples of Lynch's model (Daubin and Moran 2004; Vinogradov 2004). In chapters 3 and 7, the author reviews the mobile genetic element classes, their role in the genome evolution, and the organization of the human genome as examples. The example is described in detail and describes the mobile genetic elements; but, repeating information on mobile genetic elements in 2 chapters will not help the reader by swing back and forward. It might have been better to merge the human genome organization (Chapter 3) in the mobile genetic elements (Chapter 7). Chapter 5 discusses the importance of the noncoding futures of chromosomes and their roles to insure probable inheritance of complete genome from generation to generation, as well the special mechanisms that allow them to evolve. The author continues to show how the complexity of genomes accumulates more genetic materials by gene duplication. In chapter 8, the author describes the duplication levels, the mechanisms to preserve the duplicated genes, and how the multicellular organisms retain their duplicated genes. Based on the differences in gene structure of the prokaryotes and eukaryotes (Chapter 9) and the gene transcripts mechanisms (Chapter 10), the author illuminates how the multicellular organisms have several dozens of introns, more than the unicellular organisms, then the mechanisms of intron origin, the transcription and translation mechanisms, and the splicing process. In chapters 11 and 12, Lynch discusses the effect of nonadaptive forces on noncoding DNA (organelle genomes) and low recombination regions (sex chromosomes), respectively. Lynch proposed that organelle evolution is also controlled by random genetic drift and mutation pressure; however, the deeper understanding of nucleomorph evolution will require information on aspects of the population genetic environment associated with genomic information such as effective population size and mutation pressure. In chapter 12, Lynch stated that, even though with premature data of the sex chromosomes, the X chromosome generally does not provide a suitable environment for nonadaptive forces to evolve individual genes, in contrast to the Y chromosome. The last chapter discusses the history of population genetics and molecular evolution. This part could well have been merged with the first chapter to give the reader the essential background on the evolution of that branch of science.
The book is intended for scientists, researchers, and professionals with an interest in molecular evolution. Even though the book is presented and organized in a nontextbook style, graduate students in this discipline, with an adequate background in genetics and molecular biology, will find many chapters of this book to be a worthwhile source for studying molecular evolution. The text is good, up-to-date, and readable. Tables and figures are clear and detailed; the important points that need more explanation are discussed in detail in brown-shaded boxes. At the end of the book, there is a glossary of terms including basic and new terms in an easy and rigorous form. A comprehensive bibliography (more than 2000 references) is provided, followed by author and detailed subject indexes.
In summary, this is a good book on molecular evolution and a useful addition to the evolution library. The author has simplified the subject, so that it will be easy for the beginners in the field of molecular evolution as well as for experts to understand. It should be in the library of all institutions and colleges interested in molecular evolution and population genetics.
Center of Applied Genetic Technologies, University of Georgia, 111 Riverbend Road, Athens, GA 30605
e-mail: hussein{at}uga.edu
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Daubin V, Moran NA. Comment on "the origins of genome complexity". Science (2004) 306:978.[Medline]
Kimura M. DNA and the neutral theory. Philos Trans R Soc Lond B Biol Sci. (1986) 312:343–354.[ISI][Medline]
Lewin R. Patterns in evolution: the new molecular view. (1996) New York: Scientific American Library.
Lynch M. The origins of eukaryotic gene structure. Mol Biol Evol. (2006) 23:450–468.
Lynch M. The frailty of adaptive hypotheses for the origins of organismal complexity. Proc Natl Acad Sci USA (2007) 104:8597–8604.
Lynch M, Conery JS. The origins of genome complexity. Science (2003) 302:1401–1404.
Lynch M, Conery JS. Response to comment on "the origins of genome complexity. Science (2004) 306:978.[Medline]
Lynch M, Koskella B, Schaack S. Mutation pressure and the evolution of organelle genome architecture. Science (2006) 311:1727–1730.
Paland S, Lynch M. Transitions to asexuality result in excess amino-acid substitutions. Science (2006) 311:990–992.
Vinogradov AE. Testing genome complexity. Science (2004) 304:389–390.
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