The Evolution and Emergence of RNA Viruses Book

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