The Evolution and Emergence of RNA Viruses

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RNA viruses provide unique insights into the patterns and processes of evolutionary change in real time. The study of viral evolution is especially topical given the growing awareness that emerging and re-emerging diseases (most of which are caused by RNA viruses) represents a major threat to public health. However, while the study of viral evolution has developed rapidly in the last 30 years, relatively little attention has been directed toward linking work on the mechanisms of viral evolution within cells or individual hosts, to the epidemiological outcomes of theses processes. This novel book fills this gap by considering the patterns and processes of viral evolution across their entire range of spatial and temporal scales.

The Evolution and Emergence of RNA Viruses provides a comprehensive overview of RNA virus evolution, with a particular focus on genomic and phylogenetic approaches. This is the first book to link mechanisms of viral evolution with disease dynamic, using high-profile examples in emergence and evolution such as influenza, HIV, dengue fever, and rabies. It also reveals the underlying evolutionary processes by which emerging viruses cross species boundaries and spread in new hosts.

This advanced textbook is suitable for graduate level students taking seminars and courses in evolutionary biology, epidemiology, virology, disease ecology and population genetics, as well as academics and researchers in theses fields. Its accessible treatment of evolutionary merchanisms will also be of relevance and use to molecular epidemiologists and cellular biologists.

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Editorial Reviews

From the Publisher
"A useful addition to the bookshelves of academicians and researchers. The combination of topical examples, appropriate and useful diagrams, and manageable scope are also sure to attract young researchers and graduate-level students. Holmes manages to bring together evolutionary biology, epidemiology, virology, disease ecology, and population genetics in a clear and concise way. The book highlights the results of new computational phylogenetic approaches that have been applied to viruses and the potential they have for elucidating the mechanisms of viral evolution, which will hopefully encourage more research in the future."—Systematic Biology

"The aim of The Oxford Series in Ecology and Evolution is to stimulate ideas in new research fields, and The Evolution and Emergence of RNA Viruses is an excellent addition to this series."—TREE

"Impressive...I recommed it to those who have knowledge of and interest in the molecular biology of RNA viruses."—Brian W. J. Mahy, Emerging Infectious Diseases

"A volume that will be essential for any student of RNA virus diversity and evolution."—Quarterly Review of Biology

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Product Details

Meet the Author

Edward C. Holmes is Professor of Biology and Eberly College of Science Distinguished Senior Scholar at The Pennsylvania State University. He has authored over 200 scientific publications and in 2003 was awarded the Scientific Medal for 'Achievement in Research by a Zoologist Under the Age of 40' by the Zoological Society of London for his work on evolutionary biology and bioinformatics. He is also co-author of a highly regarded text book in molecular evolution and phylogenetics. His research sits at the interface of four disciplines - evolutionary biology, genomics, infectious disease and bioinformatics - and for the last 20 years he has been involved in the development and use of a variety of computational techniques to reveal the fundamental patterns and processes of evolutionary change in viruses.

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Table of Contents

1 Introduction 1

1.1 Why study RNA virus evolution? 1

1.1.1 Ways to study viral evolution 2

1.1.2 The scope of this book 4

1.2 RNA viruses and evolutionary biology 5

1.2.1 The RNA virus world 6

1.3 The basics of viral biology 8

1.3.1 A cursory history of virology 8

1.3.2 Virology 101 9

1.3.3 Exploring the virosphere 13

2 The origins of RNA viruses 15

2.1 Introduction 15

2.1.1 The perils of deep viral phylogeny 15

2.2 Theories for the origin of RNA viruses 16

2.2.1 The regressive origin theory 17

2.2.2 RNA viruses as escaped genes 18

2.2.3 RNA viruses and the RNA world 20

2.2.4 Eigen's paradox 22

2.2.5 The taxonomic distribution of RNA viruses 24

2.2.6 Conserved protein structures 25

2.3 Deep phylogenetic relationships among RNA viruses 28

2.3.1 The 'higher-order' relationships of RNA viruses 29

2.3.2 Phylogenies based on genome organization 34

2.3.3 Phylogenies based on protein structure 34

2.4 RNA viruses and the evolution of the genetic code 35

3 The mechanisms of RNA virus evolution 37

3.1 The evolutionary dynamics of RNA viruses 37

3.1.1 Mutation rates in RNA viruses and their determinants 37

3.1.2 A comparison of substitution rates in viruses 39

3.1.3 Differences in viral generation time 42

3.1.4 Slowly evolving RNA viruses? 43

3.1.5 Rapidly evolving ssDNA viruses 44

3.1.6 What sets the rate of RNA virus evolution? 45

3.1.7 Trade-offs and the evolution of mutation rates 46

3.1.8 Mutation rates and mutational loads 47

3.1.9 Are RNA viruses trapped by high mutation rates? 48

3.2 Recombination and reassortment in RNA virus evolution 48

3.2.1 Recombination frequency in RNA viruses 50

3.2.2 Detecting recombinationin RNA viruses 51

3.2.3 What determines the rate of recombination in RNA viruses? 52

3.2.4 Recombination and deleterious mutation 53

3.3 Natural selection, genetic drift, and the genetics of adaptation 55

3.3.1 Effective population sizes in viral evolution 56

3.3.2 Transmission bottlenecks 58

3.3.3 The dynamics of allele fixation: estimating selection coefficients 59

3.3.4 The importance of hitch-hiking 62

3.3.5 Patterns of synonymous and nonsynonymous evolution 63

3.3.6 Natural selection and transmission mode 63

3.3.7 Escape from intrinsic immunity 65

3.3.8 Strictly neutral evolution in RNA viruses? 66

3.3.9 Determinants of codon bias (and nucleotide composition) in RNA viruses 68

3.4 Deleterious mutation and RNA virus evolution 70

3.4.1 Deleterious mutation and intra-host genetic diversity 73

3.4.2 The importance of defective interfering particles and complementation 74

3.4.3 Complementation may be commonplace in RNA viruses 75

3.5 Epistasis in RNA virus evolution 77

3.5.1 Epistasis and robustness 78

3.5.2 The importance of RNA secondary structure 80

3.5.3 Convergence and pleiotropy 82

3.6 The importance of intra-host viral diversity 83

4 The RNA virus quasispecies 87

4.1 What is a quasispecies? 87

4.2 The great quasispecies debate 90

4.2.1 What's in a name: quasispecies or polymorphism? 91

4.2.2 Is quasispecies theory different from 'classical' population genetics? 92

4.2.3 Does genetic drift destroy the quasispecies? 92

4.2.4 The evidence from 'digital organisms' 93

4.2.5 Experimental tests of quasispecies theory 93

4.2.6 Comparative analyses of RNA virus quasispecies 96

4.2.7 Recombination and the quasispecies 99

4.2.8 'Memory' in viral quasispecies 99

4.3 Error thresholds, extinction thresholds, and error catastrophes 100

4.4 Concluding remarks 103

5 Comparative genomics and the macroevolution of RNA viruses 104

5.1 The evolution of genome architecture in RNA viruses 104

5.1.1 The evolution of genome size 104

5.1.2 The exceptions: coronaviruses and roniviruses 107

5.1.3 The evolution of genome organization: an overview 109

5.1.4 The evolution of genome segmentation 111

5.1.5 The evolution of genome orientation and dsRNA viruses 113

5.1.6 The evolution of overlapping reading frames 114

5.2 The processes of genome evolution 116

5.2.1 Gene duplication in RNA virus evolution 117

5.2.2 LGT among viruses and hosts 118

5.2.3 Modular evolution 119

5.3 Patterns and processes of macroevolution in RNA viruses 120

5.3.1 Speciation in RNA viruses 121

5.3.2 A birth-death model of viral evolution 124

5.3.3 The birth and death of endogenous retroviruses 128

6 The molecular epidemiology, phylogeography, and emergence of RNA viruses 131

6.1 Phylodynamics; linking viral evolution at the phylogenetic and epidemiological scales 131

6.1.1 Coalescent approaches to viral epidemiology 133

6.2 Cross-species transmission, co-divergence, and emergence 135

6.2.1 The RNA/DNA divide again 135

6.2.2 Inferring co-divergence 137

6.2.3 The evolution of persistence in RNA viruses 138

6.2.4 Host phylogeny and viral emergence 139

6.3 The evolutionary genetics of viral emergence 142

6.3.1 Adaptation and emergence 142

6.3.2 'Off-the-shelf emergence 144

6.3.3 The fitness landscapes of emergence 146

6.3.4 Recombination, reassortment, and viral emergence 147

6.4 The phylogeography of human viruses 148

6.4.1 Viruses differ in phylogeographic pattern 149

6.5 Major transitions in human ecology and viral evolution 153

6.5.1 The transitions 154

6.5.2 Immunodeficiency and disease emergence 155

7 Case studies in RNA virus evolution and emergence 156

7.1 The evolutionary biology of influenza virus 156

7.1.1 The diversity of influenza virus 156

7.1.2 The evolution of avian influenza virus 158

7.1.3 Antigenic drift and shift 161

7.1.4 Antigenic cartography and the punctuated evolution of HA 162

7.1.5 Genome-wide evolutionary processes 165

7.2 The emergence and evolution of HIV 167

7.2.1 A brief history of HIV/AIDS 167

7.2.2 The genetic diversity of HIV 169

7.2.3 What and why are subtypes? 172

7.2.4 The origins and spread of HIV 173

7.2.5 The intra- and inter-host evolutionary dynamics of HIV 176

7.2.6 The great obsession moves to HIV 177

7.2.7 Epidemiological scale dynamics 178

7.3 The evolution of dengue virus 180

7.3.1 The origins of DENV 182

7.3.2 DENV biodiversity 184

7.3.3 Lineage birth-death in DENV 186

7.3.4 DENV fitness 187

7.3.5 Comparing dengue and yellow fever 188

7.3.6 Why no yellow fever in Asia? 190

7.4 The phylogeography and evolution of rabies virus 191

7.4.1 The world of lyssaviruses 192

7.4.2 The spatiotemporal dynamics of RABV 195

8 Epilogue 198

References 201

Index 209

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