Bats and Viruses: A New Frontier of Emerging Infectious Diseases

<p>List of Contributors xiii</p>
<p>Preface xv</p>
<p>1 THE UNIQUENESS OF BATS 1<br />Paul A. Racey</p>
<p>1.1 Introduction 1</p>
<p>1.2 Flight 2</p>
<p>1.3 Echolocation 4</p>
<p>1.4 Communication 5</p>
<p>1.5 Foraging, Diet, and Ecosystem Services 5</p>
<p>1.6 Heterothermy, Daily Torpor, and Hibernation 7</p>
<p>1.7 Reproduction 8</p>
<p>1.8 Life History Strategies 9</p>
<p>1.9 Roosting Ecology 9</p>
<p>1.9.1 Caves 9</p>
<p>1.9.2 Trees 10</p>
<p>1.9.3 Houses 10</p>
<p>1.9.4 Foliage 10</p>
<p>1.9.5 Roosts of other species 11</p>
<p>1.9.6 Roost fidelity 11</p>
<p>1.10 Migration 11</p>
<p>1.11 Climate Change 12</p>
<p>1.12 Disease ]Related Mortality 13</p>
<p>1.13 Conservation and Disease Surveillance 14</p>
<p>Acknowledgment 14</p>
<p>References 15</p>
<p>2 VIRUSES IN BATS: A HISTORIC REVIEW 23<br />Charles H. Calisher</p>
<p>2.1 Introduction 23</p>
<p>2.2 Knowledge of Bats, Background 25</p>
<p>2.3 Early, Somewhat Random Bat Virus Discoveries 25</p>
<p>2.4 More Recent Bat Virus Discoveries 27</p>
<p>2.4.1 Marburg and Ebola viruses (order Mononegavirales, family Filoviridae, genera Ebolavirus and Marburgvirus, respectively) 27</p>
<p>2.4.2 Hendra and Nipah viruses (order Mononegavirales, family Paramyxoviridae, genus Henipavirus), and other</p>
<p>paramyxoviruses 28</p>
<p>2.4.3 Coronaviruses (order Nidovirales, family Coronaviridae, genus Coronavirus) 30</p>
<p>2.4.4 Other viruses detected in bats 31</p>
<p>2.5 Summary 36</p>
<p>Acknowledgments 41</p>
<p>References 41</p>
<p>3 BAT LYSSAVIRUSES 47<br />Ivan V. Kuzmin and Charles E. Rupprecht</p>
<p>3.1 Lyssavirus Genus 47</p>
<p>3.2 Pathobiology 54</p>
<p>3.3 Surveillance and Diagnosis 57</p>
<p>3.4 General Biological Considerations on Bat Rabies 59</p>
<p>3.5 Global Distribution of Bat Lyssaviruses 62</p>
<p>3.5.1 The Americas 62</p>
<p>3.5.2 Africa 69</p>
<p>3.5.3 Eurasia 72</p>
<p>3.5.4 Australia 78</p>
<p>3.6 Public Health and Veterinary Significance of Bat Rabies 80</p>
<p>3.7 Conclusions 84</p>
<p>References 85</p>
<p>4 BAT PARAMYXOVIRUSES 99<br />Danielle E. Anderson and Glenn A. Marsh</p>
<p>4.1 Introduction to the Paramyxoviridae 99</p>
<p>4.1.1 Virus structure 100</p>
<p>4.1.2 Genome organization 101</p>
<p>4.1.3 Paramyxovirus replication 103</p>
<p>4.2 Bats as a Major Source of New Paramyxoviruses 105</p>
<p>4.2.1 Sampling methods 105</p>
<p>4.2.2 Methodologies utilized in the detection and characterization of paramyxoviruses 106</p>
<p>4.3 Known Bat Paramyxoviruses 109</p>
<p>4.3.1 Hendra virus (HeV) 109</p>
<p>4.3.2 Nipah virus (NiV) 111</p>
<p>4.3.3 Menangle virus (MenPV) 112</p>
<p>4.3.4 Cedar virus (CedPV) 113</p>
<p>4.3.5 Mapuera virus (MprPV) 114</p>
<p>4.3.6 Porcine rubulavirus (PorPV) 114</p>
<p>4.3.7 Tioman virus (TioPV) 114</p>
<p>4.3.8 Achimota viruses (AchPV) 114</p>
<p>4.3.9 Tukoko viruses (ThkPV) 115</p>
<p>4.3.10 Sosuga virus (SosPV) 115</p>
<p>4.3.11 Other paramyxoviruses 115</p>
<p>4.4 Risks, Control, and Prevention 116</p>
<p>4.4.1 Risk of spillover 116</p>
<p>4.4.2 Reservoir host management 117</p>
<p>4.4.3 Vaccines 117</p>
<p>4.5 Conclusions 118</p>
<p>Acknowledgments 118</p>
<p>References 118</p>
<p>5 BAT CORONAVIRUSES 127<br />Xing ]Yi Ge, Ben Hu, and Zheng ]Li Shi</p>
<p>5.1 Introduction 127</p>
<p>5.2 Human Diseases Related to Bat Coronaviruses 134</p>
<p>5.2.1 SARS 134</p>
<p>5.2.2 Middle East respiratory syndrome (MERS) 140</p>
<p>5.3 Genetic Diversity of Bat Coronaviruses 142</p>
<p>5.3.1 Alphacoronaviruses 142</p>
<p>5.3.2 Betacoronaviruses 145</p>
<p>5.3.3 Gammacoronaviruses 146</p>
<p>5.3.4 Classification of coronaviruses 146</p>
<p>5.4 Conclusions 147</p>
<p>Acknowledgments 148</p>
<p>References 148</p>
<p>6 BAT FILOVIRUSES 157<br />Gael Darren Maganga, Virginie Rougeron, and Eric Maurice Leroy</p>
<p>6.1 Introduction 157</p>
<p>6.2 Marburgvirus Outbreaks 158</p>
<p>6.3 Ebolavirus Outbreaks 159</p>
<p>6.3.1 Ebolavirus and Sudan ebolavirus 159</p>
<p>6.3.2 Tai Forest and Bundibugyo ebolaviruses 160</p>
<p>6.3.3 Reston ebolavirus 160</p>
<p>6.4 Filoviruses in Yinpterochiropteran Bats 160</p>
<p>6.4.1 Ebolaviruses 161</p>
<p>6.4.2 Marburgvirus 161</p>
<p>6.5 Filoviruses in Yangochiroptera Bats 163</p>
<p>6.5.1 Ebolaviruses 163</p>
<p>6.5.2 Marburgvirus 163</p>
<p>6.5.3 Cuevavirus 163</p>
<p>6.6 Ecological and Epidemiological Patterns in Bats 164</p>
<p>6.6.1 An extended natural geographic distribution 164</p>
<p>6.6.2 Bats as drivers of filoviruses emergence and spillover? 164</p>
<p>6.6.3 Uncertainty surrounding the identification of the Lloviu virus reservoir 167</p>
<p>6.7 Bat Filovirus Characterization 167</p>
<p>6.7.1 Filovirus isolation 167</p>
<p>6.7.2 Filovirus RNA detection 168</p>
<p>6.7.3 Filovirus antigen detection 168</p>
<p>6.7.4 Whole genome amplification 168</p>
<p>6.8 Conclusions 169</p>
<p>Acknowledgments 170</p>
<p>References 170</p>
<p>7 BATS AND REVERSE TRANSCRIBING RNA AND DNA VIRUSES 177<br />Gilda Tachedjian, Joshua A. Hayward, and Jie Cui</p>
<p>7.1 Introduction to Reverse Transcribing RNA and DNA Viruses 177</p>
<p>7.1.1 Retroviruses 177</p>
<p>7.1.2 Hepadnaviruses 180</p>
<p>7.2 Endogenous Retroviruses in Bats 181</p>
<p>7.2.1 Endogenous retroviruses: A transposable element subclass 181</p>
<p>7.2.2 Endogenous retroviruses originate from exogenous retroviruses 182</p>
<p>7.2.3 Endogenous retrovirus nomenclature 182</p>
<p>7.2.4 Role of transposable elements and endogenous retroviruses in disease and host evolution 183</p>
<p>7.2.5 Endogenous retroviruses as fossil records of ancient exogenous retroviruses</p>
<p>184</p>
<p>7.3 Gammaretroviruses in Bats of Different Suborders 184</p>
<p>7.3.1 Gammaretroviruses: host range and diseases 184</p>
<p>7.3.2 Discovery of gammaretroviruses in bats 185</p>
<p>7.4 Betaretroviruses in Bats of Different Suborders 187</p>
<p>7.4.1 Betaretroviruses: host range and diseases 187</p>
<p>7.4.2 Betaretroviruses in bat transcriptomes and genomes 188</p>
<p>7.4.3 Extensive diversity among bat betaretroviruses 188</p>
<p>7.5 Pathogenic Hepadnaviruses Related to HBV in Bats 191</p>
<p>7.6 Bat Metagenomics Studies 192</p>
<p>7.7 Bats as Potential Reservoirs for Retroviral and Hepadnaviral Zoonoses 194</p>
<p>7.8 Conclusions 195</p>
<p>Acknowledgments 196</p>
<p>References 196</p>
<p>8 BAT REOVIRUSES 203<br />Claudia Kohl and Andreas Kurth</p>
<p>8.1 Introduction 203</p>
<p>8.1.1 Background 203</p>
<p>8.1.2 Reovirus taxonomy and disease epidemiology 203</p>
<p>8.2 Orthoreoviruses of Bats and Humans 206</p>
<p>8.2.1 Nelson Bay orthoreovirus 206</p>
<p>8.2.2 Other bat ]related orthoreoviruses 210</p>
<p>8.3 Bat Orbiviruses 211</p>
<p>8.4 Bat Rotaviruses 211</p>
<p>8.5 Zoonotic Potential of Bat Reoviruses 213</p>
<p>Acknowledgments 213</p>
<p>References 213</p>
<p>9 OTHER BAT ]BORNE VIRUSES 217<br />Krista Queen, Mang Shi, Larry J. Anderson, and Suxiang Tong</p>
<p>9.1 Introduction 217</p>
<p>9.2 RNA Viruses 218</p>
<p>9.2.1 Influenza viruses 218</p>
<p>9.2.2 Alphaviruses 227</p>
<p>9.2.3 Bunyaviruses 227</p>
<p>9.2.4 Flaviviruses 229</p>
<p>9.2.5 Arenaviruses 231</p>
<p>9.2.6 Picornaviruses 231</p>
<p>9.2.7 Astroviruses 233</p>
<p>9.2.8 Caliciviruses 234</p>
<p>9.3 DNA Viruses 234</p>
<p>9.3.1 Adenoviruses 234</p>
<p>9.3.2 Herpesviruses 235</p>
<p>9.3.3 Poxviruses 236</p>
<p>9.3.4 Polyomaviruses 236</p>
<p>9.3.5 Parvoviruses 237</p>
<p>9.3.6 Papillomaviruses 238</p>
<p>9.4 Conclusions 238</p>
<p>References 239</p>
<p>10 ANTHROPOGENIC EPIDEMICS: THE ECOLOGY OF BAT ]BORNE VIRUSES AND OUR ROLE IN THEIR EMERGENCE 249<br />Jonathan H. Epstein and Hume E. Field</p>
<p>10.1 Introduction 249</p>
<p>10.2 The Bat Human and Bat Livestock Interface: The Importance of Disease Ecology 250</p>
<p>10.3 Approaches to Understanding the Ecology of Bat ]Borne Viruses 253</p>
<p>10.3.1 Observational study design 254</p>
<p>10.3.2 Mathematical models 257</p>
<p>10.3.3 Outbreak response and long ]term ecological study 258</p>
<p>10.4 Anthropogenic Activities Drive Zoonotic Disease Emergence from Bats 263</p>
<p>10.4.1 Agricultural expansion/intensification: Nipah virus 263</p>
<p>10.4.2 Urbanization: Hendra virus 266</p>
<p>10.4.3 Wildlife trade: SARS ]CoV 268</p>
<p>10.4.4 Bushmeat hunting: Ebola virus 271</p>
<p>10.5 Outbreak Mitigation: Managing the Interface 272</p>
<p>10.6 Conclusions 273</p>
<p>Acknowledgments 274</p>
<p>References 274</p>
<p>11 ARE BATS REALLY SPECIAL AS VIRAL RESERVOIRS? WHAT WE KNOW AND NEED TO KNOW 281<br />Kevin J. Olival, Cristin C. Weekley, and Peter Daszak</p>
<p>11.1 Introduction 281</p>
<p>11.2 What Factors May Make a Host Taxon Special as a Viral Reservoir? 282</p>
<p>11.3 Factors that May Confound Investigations of Whether or Not a Taxonomic Group is Special 282</p>
<p>11.3.1 Research bias towards certain hosts and pathogens 282</p>
<p>11.3.2 Lack of thorough disease ecology studies 283</p>
<p>11.3.3 The ability to measure immune responses and detect illness in hosts 284</p>
<p>11.4 Viral Diversity in Bats Compared to other Mammalian Hosts 286</p>
<p>11.4.1 Do bats harbor a disproportionate number of viruses? 286</p>
<p>11.4.2 Do bats harbor a disproportionate number of zoonoses? 286</p>
<p>11.4.3 Focused literature review of bat viral discovery efforts from the past 7 years 288</p>
<p>11.5 Life History Traits: Are Bats Unique? 288</p>
<p>11.6 Distribution and Diversity of Bat Viruses, and Ways to Target Future Discovery Efforts 291</p>
<p>11.7 Summary and Future Research 292</p>
<p>References 293</p>
<p>12 ANIMAL MODELS OF RECENTLY EMERGED BAT ]BORNE VIRUSES 295<br />Jackie A. Pallister and Deborah J. Middleton</p>
<p>12.1 Introduction 295</p>
<p>12.2 SARS Coronavirus 296</p>
<p>12.2.1 Human disease 296</p>
<p>12.2.2 Small animal models 296</p>
<p>12.2.3 Nonhuman primates 298</p>
<p>12.2.4 Spillover hosts 298</p>
<p>12.2.5 Reservoir host 298</p>
<p>12.3 Filoviruses 299</p>
<p>12.3.1 Human disease 299</p>
<p>12.3.2 Small animal models 300</p>
<p>12.3.3 Nonhuman primates 300</p>
<p>12.3.4 Spillover hosts 301</p>
<p>12.3.5 Reservoir host 302</p>
<p>12.4 Paramyxoviruses 302</p>
<p>12.4.1 Human disease 302</p>
<p>12.4.2 Small animal models 303</p>
<p>12.4.3 Nonhuman primates 304</p>
<p>12.4.4 Spillover hosts 305</p>
<p>12.4.5 Reservoir host 305</p>
<p>12.5 Conclusions 306</p>
<p>References 306</p>
<p>13 BAT GENOMICS 315<br />James W. Wynne and Mary Tachedjian</p>
<p>13.1 Introduction 315</p>
<p>13.2 Genomics 316</p>
<p>13.2.1 The era of bat genomics 316</p>
<p>13.2.2 Phylogenomics 317</p>
<p>13.2.3 Immunity 317</p>
<p>13.2.4 Gene family expansion 319</p>
<p>13.2.5 Longevity 319</p>
<p>13.2.6 Hibernation 320</p>
<p>13.2.7 Echolocation and convergent evolution 320</p>
<p>13.2.8 Genomic adaptations associated with flight 321</p>
<p>13.2.9 Limitations of genome sequencing 321</p>
<p>13.3 Transcriptomics and MicroRNAs 322</p>
<p>13.3.1 Cataloging immune genes 322</p>
<p>13.3.2 Functional genomics of echolocation 323</p>
<p>13.3.3 MicroRNA discovery 323</p>
<p>13.3.4 Bat specific gene discovery through transcriptomics 323</p>
<p>13.4 Conclusions 324</p>
<p>References 324</p>
<p>14 BAT IMMUNOLOGY 327<br />Michelle L. Baker and Peng Zhou</p>
<p>14.1 Introduction 327</p>
<p>14.2 Immune Tissues and Cells 328</p>
<p>14.3 Innate Immunity 329</p>
<p>14.3.1 Pattern recognition receptors (PRRs) 329</p>
<p>14.3.2 Interferon (IFN) family members 330</p>
<p>14.3.3 Production of IFNs by bat cells 331</p>
<p>14.3.4 IFN receptors and downstream signaling molecules 333</p>
<p>14.3.5 Interferon stimulated genes (ISGs) 334</p>
<p>14.3.6 MicroRNAs 335</p>
<p>14.4 Adaptive Immunity 335</p>
<p>14.4.1 Immunoglobulins 336</p>
<p>14.4.2 Antibody mediated immune responses to experimental viral infections 336</p>
<p>14.4.3 Maternally derived antibody protection 338</p>
<p>14.4.4 T ]cell ]mediated immune responses 339</p>
<p>14.4.5 The major histocompatibility complex (MHC) 340</p>
<p>14.4.6 Cytokines 340</p>
<p>14.5 Conclusions 341</p>
<p>References 342</p>
<p>Species Index 349</p>
<p>Subject Index 361</p>