Bats and Viruses

Edited by Lin-Fa Wang is Director of the Program in Emerging Infectious Diseases at Duke-NUS Graduate Medical School, Singapore, and an Office of the Chief Executive Science Leader at CSIRO Australian Animal Health Laboratory in Geelong, Victoria, Australia Christopher Cowled is a Research Scientist at the CSIRO Australian Animal Health Laboratory in Geelong, Victoria, Australia  

List of Contributors xiii

Preface xv

1 THE UNIQUENESS OF BATS 1
Paul A. Racey

1.1 Introduction 1

1.2 Flight 2

1.3 Echolocation 4

1.4 Communication 5

1.5 Foraging, Diet, and Ecosystem Services 5

1.6 Heterothermy, Daily Torpor, and Hibernation 7

1.7 Reproduction 8

1.8 Life History Strategies 9

1.9 Roosting Ecology 9

1.9.1 Caves 9

1.9.2 Trees 10

1.9.3 Houses 10

1.9.4 Foliage 10

1.9.5 Roosts of other species 11

1.9.6 Roost fidelity 11

1.10 Migration 11

1.11 Climate Change 12

1.12 Disease]Related Mortality 13

1.13 Conservation and Disease Surveillance 14

Acknowledgment 14

References 15

2 VIRUSES IN BATS: A HISTORIC REVIEW 23
Charles H. Calisher

2.1 Introduction 23

2.2 Knowledge of Bats, Background 25

2.3 Early, Somewhat Random Bat Virus Discoveries 25

2.4 More Recent Bat Virus Discoveries 27

2.4.1 Marburg and Ebola viruses (order Mononegavirales, family Filoviridae, genera Ebolavirus and Marburgvirus, respectively) 27

2.4.2 Hendra and Nipah viruses (order Mononegavirales, family Paramyxoviridae, genus Henipavirus), and other

paramyxoviruses 28

2.4.3 Coronaviruses (order Nidovirales, family Coronaviridae, genus Coronavirus) 30

2.4.4 Other viruses detected in bats 31

2.5 Summary 36

Acknowledgments 41

References 41

3 BAT LYSSAVIRUSES 47
Ivan V. Kuzmin and Charles E. Rupprecht

3.1 Lyssavirus Genus 47

3.2 Pathobiology 54

3.3 Surveillance and Diagnosis 57

3.4 General Biological Considerations on Bat Rabies 59

3.5 Global Distribution of Bat Lyssaviruses 62

3.5.1 The Americas 62

3.5.2 Africa 69

3.5.3 Eurasia 72

3.5.4 Australia 78

3.6 Public Health and Veterinary Significance of Bat Rabies 80

3.7 Conclusions 84

References 85

4 BAT PARAMYXOVIRUSES 99
Danielle E. Anderson and Glenn A. Marsh

4.1 Introduction to the Paramyxoviridae 99

4.1.1 Virus structure 100

4.1.2 Genome organization 101

4.1.3 Paramyxovirus replication 103

4.2 Bats as a Major Source of New Paramyxoviruses 105

4.2.1 Sampling methods 105

4.2.2 Methodologies utilized in the detection and characterization of paramyxoviruses 106

4.3 Known Bat Paramyxoviruses 109

4.3.1 Hendra virus (HeV) 109

4.3.2 Nipah virus (NiV) 111

4.3.3 Menangle virus (MenPV) 112

4.3.4 Cedar virus (CedPV) 113

4.3.5 Mapuera virus (MprPV) 114

4.3.6 Porcine rubulavirus (PorPV) 114

4.3.7 Tioman virus (TioPV) 114

4.3.8 Achimota viruses (AchPV) 114

4.3.9 Tukoko viruses (ThkPV) 115

4.3.10 Sosuga virus (SosPV) 115

4.3.11 Other paramyxoviruses 115

4.4 Risks, Control, and Prevention 116

4.4.1 Risk of spillover 116

4.4.2 Reservoir host management 117

4.4.3 Vaccines 117

4.5 Conclusions 118

Acknowledgments 118

References 118

5 BAT CORONAVIRUSES 127
Xing]Yi Ge, Ben Hu, and Zheng]Li Shi

5.1 Introduction 127

5.2 Human Diseases Related to Bat Coronaviruses 134

5.2.1 SARS 134

5.2.2 Middle East respiratory syndrome (MERS) 140

5.3 Genetic Diversity of Bat Coronaviruses 142

5.3.1 Alphacoronaviruses 142

5.3.2 Betacoronaviruses 145

5.3.3 Gammacoronaviruses 146

5.3.4 Classification of coronaviruses 146

5.4 Conclusions 147

Acknowledgments 148

References 148

6 BAT FILOVIRUSES 157
Gael Darren Maganga, Virginie Rougeron, and Eric Maurice Leroy

6.1 Introduction 157

6.2 Marburgvirus Outbreaks 158

6.3 Ebolavirus Outbreaks 159

6.3.1 Ebolavirus and Sudan ebolavirus 159

6.3.2 Tai Forest and Bundibugyo ebolaviruses 160

6.3.3 Reston ebolavirus 160

6.4 Filoviruses in Yinpterochiropteran Bats 160

6.4.1 Ebolaviruses 161

6.4.2 Marburgvirus 161

6.5 Filoviruses in Yangochiroptera Bats 163

6.5.1 Ebolaviruses 163

6.5.2 Marburgvirus 163

6.5.3 Cuevavirus 163

6.6 Ecological and Epidemiological Patterns in Bats 164

6.6.1 An extended natural geographic distribution 164

6.6.2 Bats as drivers of filoviruses emergence and spillover? 164

6.6.3 Uncertainty surrounding the identification of the Lloviu virus reservoir 167

6.7 Bat Filovirus Characterization 167

6.7.1 Filovirus isolation 167

6.7.2 Filovirus RNA detection 168

6.7.3 Filovirus antigen detection 168

6.7.4 Whole genome amplification 168

6.8 Conclusions 169

Acknowledgments 170

References 170

7 BATS AND REVERSE TRANSCRIBING RNA AND DNA VIRUSES 177
Gilda Tachedjian, Joshua A. Hayward, and Jie Cui

7.1 Introduction to Reverse Transcribing RNA and DNA Viruses 177

7.1.1 Retroviruses 177

7.1.2 Hepadnaviruses 180

7.2 Endogenous Retroviruses in Bats 181

7.2.1 Endogenous retroviruses: A transposable element subclass 181

7.2.2 Endogenous retroviruses originate from exogenous retroviruses 182

7.2.3 Endogenous retrovirus nomenclature 182

7.2.4 Role of transposable elements and endogenous retroviruses in disease and host evolution 183

7.2.5 Endogenous retroviruses as fossil records of ancient exogenous retroviruses

184

7.3 Gammaretroviruses in Bats of Different Suborders 184

7.3.1 Gammaretroviruses: host range and diseases 184

7.3.2 Discovery of gammaretroviruses in bats 185

7.4 Betaretroviruses in Bats of Different Suborders 187

7.4.1 Betaretroviruses: host range and diseases 187

7.4.2 Betaretroviruses in bat transcriptomes and genomes 188

7.4.3 Extensive diversity among bat betaretroviruses 188

7.5 Pathogenic Hepadnaviruses Related to HBV in Bats 191

7.6 Bat Metagenomics Studies 192

7.7 Bats as Potential Reservoirs for Retroviral and Hepadnaviral Zoonoses 194

7.8 Conclusions 195

Acknowledgments 196

References 196

8 BAT REOVIRUSES 203
Claudia Kohl and Andreas Kurth

8.1 Introduction 203

8.1.1 Background 203

8.1.2 Reovirus taxonomy and disease epidemiology 203

8.2 Orthoreoviruses of Bats and Humans 206

8.2.1 Nelson Bay orthoreovirus 206

8.2.2 Other bat]related orthoreoviruses 210

8.3 Bat Orbiviruses 211

8.4 Bat Rotaviruses 211

8.5 Zoonotic Potential of Bat Reoviruses 213

Acknowledgments 213

References 213

9 OTHER BAT]BORNE VIRUSES 217
Krista Queen, Mang Shi, Larry J. Anderson, and Suxiang Tong

9.1 Introduction 217

9.2 RNA Viruses 218

9.2.1 Influenza viruses 218

9.2.2 Alphaviruses 227

9.2.3 Bunyaviruses 227

9.2.4 Flaviviruses 229

9.2.5 Arenaviruses 231

9.2.6 Picornaviruses 231

9.2.7 Astroviruses 233

9.2.8 Caliciviruses 234

9.3 DNA Viruses 234

9.3.1 Adenoviruses 234

9.3.2 Herpesviruses 235

9.3.3 Poxviruses 236

9.3.4 Polyomaviruses 236

9.3.5 Parvoviruses 237

9.3.6 Papillomaviruses 238

9.4 Conclusions 238

References 239

10 ANTHROPOGENIC EPIDEMICS: THE ECOLOGY OF BAT]BORNE VIRUSES AND OUR ROLE IN THEIR EMERGENCE 249
Jonathan H. Epstein and Hume E. Field

10.1 Introduction 249

10.2 The Bat–Human and Bat–Livestock Interface: The Importance of Disease Ecology 250

10.3 Approaches to Understanding the Ecology of Bat]Borne Viruses 253

10.3.1 Observational study design 254

10.3.2 Mathematical models 257

10.3.3 Outbreak response and long]term ecological study 258

10.4 Anthropogenic Activities Drive Zoonotic Disease Emergence from Bats 263

10.4.1 Agricultural expansion/intensification: Nipah virus 263

10.4.2 Urbanization: Hendra virus 266

10.4.3 Wildlife trade: SARS]CoV 268

10.4.4 Bushmeat hunting: Ebola virus 271

10.5 Outbreak Mitigation: Managing the Interface 272

10.6 Conclusions 273

Acknowledgments 274

References 274

11 ARE BATS REALLY “SPECIAL” AS VIRAL RESERVOIRS? WHAT WE KNOW AND NEED TO KNOW 281
Kevin J. Olival, Cristin C. Weekley, and Peter Daszak

11.1 Introduction 281

11.2 What Factors May Make a Host Taxon “Special” as a Viral Reservoir? 282

11.3 Factors that May Confound Investigations of Whether or Not a Taxonomic Group is “Special” 282

11.3.1 Research bias towards certain hosts and pathogens 282

11.3.2 Lack of thorough disease ecology studies 283

11.3.3 The ability to measure immune responses and detect illness in hosts 284

11.4 Viral Diversity in Bats Compared to other Mammalian Hosts 286

11.4.1 Do bats harbor a disproportionate number of viruses? 286

11.4.2 Do bats harbor a disproportionate number of zoonoses? 286

11.4.3 Focused literature review of bat viral discovery efforts from the past 7 years 288

11.5 Life History Traits: Are Bats Unique? 288

11.6 Distribution and Diversity of Bat Viruses, and Ways to Target Future Discovery Efforts 291

11.7 Summary and Future Research 292

References 293

12 ANIMAL MODELS OF RECENTLY EMERGED BAT]BORNE VIRUSES 295
Jackie A. Pallister and Deborah J. Middleton

12.1 Introduction 295

12.2 SARS Coronavirus 296

12.2.1 Human disease 296

12.2.2 Small animal models 296

12.2.3 Nonhuman primates 298

12.2.4 Spillover hosts 298

12.2.5 Reservoir host 298

12.3 Filoviruses 299

12.3.1 Human disease 299

12.3.2 Small animal models 300

12.3.3 Nonhuman primates 300

12.3.4 Spillover hosts 301

12.3.5 Reservoir host 302

12.4 Paramyxoviruses 302

12.4.1 Human disease 302

12.4.2 Small animal models 303

12.4.3 Nonhuman primates 304

12.4.4 Spillover hosts 305

12.4.5 Reservoir host 305

12.5 Conclusions 306

References 306

13 BAT GENOMICS 315
James W. Wynne and Mary Tachedjian

13.1 Introduction 315

13.2 Genomics 316

13.2.1 The era of bat genomics 316

13.2.2 Phylogenomics 317

13.2.3 Immunity 317

13.2.4 Gene family expansion 319

13.2.5 Longevity 319

13.2.6 Hibernation 320

13.2.7 Echolocation and convergent evolution 320

13.2.8 Genomic adaptations associated with flight 321

13.2.9 Limitations of genome sequencing 321

13.3 Transcriptomics and MicroRNAs 322

13.3.1 Cataloging immune genes 322

13.3.2 Functional genomics of echolocation 323

13.3.3 MicroRNA discovery 323

13.3.4 Bat specific gene discovery through transcriptomics 323

13.4 Conclusions 324

References 324

14 BAT IMMUNOLOGY 327
Michelle L. Baker and Peng Zhou

14.1 Introduction 327

14.2 Immune Tissues and Cells 328

14.3 Innate Immunity 329

14.3.1 Pattern recognition receptors (PRRs) 329

14.3.2 Interferon (IFN) family members 330

14.3.3 Production of IFNs by bat cells 331

14.3.4 IFN receptors and downstream signaling molecules 333

14.3.5 Interferon stimulated genes (ISGs) 334

14.3.6 MicroRNAs 335

14.4 Adaptive Immunity 335

14.4.1 Immunoglobulins 336

14.4.2 Antibody mediated immune responses to experimental viral infections 336

14.4.3 Maternally derived antibody protection 338

14.4.4 T]cell]mediated immune responses 339

14.4.5 The major histocompatibility complex (MHC) 340

14.4.6 Cytokines 340

14.5 Conclusions 341

References 342

Species Index 349

Subject Index 361