The Origins of Genome Architecture

Abstract

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 examp