Preface ...................................................... xvii
1 Parasites and humans ......................................... 1
1.1 Mission impossible ...................................... 1
1.2 Some lessons provided by yellow fever ................... 3
1.2.1 The parasite life-cycle can be complex ........... 4
1.2.2 Not all host and parasite strains are the same ... 4
1.2.3 Complex physiological and molecular mechanisms
underlie the infection ........................... 4
1.2.4 Parasites and hosts are populations .............. 5
1.2.5 Parasites can be controlled when we understand
them ............................................. 5
1.3 Parasites in our times .................................. 6
Summary ...................................................... 8
2 The study of evolutionary parasitology ....................... 9
2.1 The evolutionary process ................................ 9
2.2 Questions about host-parasite interactions ............. 12
2.3 Selection and units that evolve ........................ 13
2.4 Life history ........................................... 14
2.5 Studying adaptation: optimality and evolutionarily
stable strategies (ESS) ................................ 14
2.5.1 Optimality ...................................... 15
2.5.2 Evolutionarily stable strategies (ESS) .......... 16
2.6 Comparative studies .................................... 16
Summary ..................................................... 17
3 The diversity and natural history of parasites .............. 18
3.1 The ubiquity of parasites .............................. 18
3.2 A systematic overview of parasites ..................... 20
3.2.1 Viruses ......................................... 20
3.2.2 Prokaryotes ..................................... 21
3.2.2.1 Archaea ................................ 22
3.2.2.2 Bacteria ............................... 22
3.2.3 The basal Eukaryotes ............................ 24
3.2.4 Protozoa ........................................ 24
3.2.4.1 Mastigophora ........................... 25
3.2.4.2 Sarcodina .............................. 25
3.2.4.3 Sporozoa ............................... 26
3.2.4.4 Ciliophora ............................. 26
3.2.5 Fungi ........................................... 27
3.2.6 Nematodes (roundworms) .......................... 28
3.2.7 Flatworms ....................................... 29
3.2.8 Acanthocephala .................................. 30
3.2.9 Annelida ........................................ 30
3.2.10 Crustacea ....................................... 31
3.2.10.1 Pentastomida ........................... 31
3.2.10.2 Copepods ............................... 31
3.2.10.3 Isopods ................................ 31
3.2.10.4 Branchiura (fish lice) ................. 31
3.2.10.5 Other groups ........................... 31
3.2.11 Mites (Acari), ticks, lice (Mallophaga,
Anoplura) ....................................... 32
3.2.12 Parasitic insects (parasitoids) ................. 33
3.3 The evolution of parasitism ............................ 33
3.3.1 Evolution of parasitism in nematodes ............ 34
3.3.2 Evolution of parasitism in trypanosomes ......... 35
3.4 The diversity and evolution of parasite life-cycles .... 38
3.4.1 Steps in a parasite's life-cycle ................ 38
3.4.1.1 Step 7: finding a host ................. 38
3.4.1.1.1 Passive dispersion .......... 38
3.4.1.1.2 Active host-finding ......... 39
3.4.1.2 Step 2: infecting and establishment
in the host ............................ 39
3.4.1.2 Step 3: growth, multiplication ......... 39
3.4.1.3 Step 4: reproduction ................... 40
3.4.1.4 Step 5: transmission ................... 40
3.4.2 Modes of transmission ........................... 40
3.4.2.1 Direct transmission .................... 40
3.4.2.2 Transmission with paratenic hosts ...... 40
3.4.2.3 Vector transmission .................... 42
3.4.3 Trematode life-cycles ........................... 42
3.4.4 The evolution of complex parasite life-cycles ... 46
Summary ..................................................... 51
4 The natural history of defences ............................. 52
4.1 The defence sequence ................................... 52
4.1.1 Pre-infection defences .......................... 52
4.1.1.1 Spatial avoidance ...................... 52
4.1.1.2 Temporal avoidance ..................... 53
4.1.1.3 Avoiding certain diets ................. 53
4.1.1.4 The selfish herd ....................... 55
4.1.1.5 Mating behaviour and mate choice ....... 55
4.1.1.6 Self-medication ........................ 55
4.1.1.7 Anticipatory defences .................. 55
4.1.1.8 Genetic defences ....................... 55
4.1.2 Post-infection defences ......................... 55
4.1.2.1 Behavioural changes .................... 56
4.1.2.2 Grooming ............................... 56
4.1.2.3 Fever and chilling ..................... 57
4.1.3 Social immunity ................................. 57
4.2 Defence by the immune system ........................... 59
4.3 Basic elements of the immune defence ................... 60
4.3.1 Humoral and cellular defences ................... 60
4.3.1.1 Phagocytosis ........................... 62
4.3.1.2 Melanization, encapsulation ............ 64
4.3.1.2 Clotting, nodule formation ............. 64
4.3.1.2 Inflammation ........................... 65
4.3.2 Innate and adaptive (acquired) immunity ......... 65
4.3.2.1 Innate immune defence .................. 65
4.3.2.2 Adaptive (acquired) immunity ........... 65
4.3.3 Signalling cascades ............................. 66
4.3.3.1 Plants ................................. 68
4.3.3.2 Insects ................................ 68
4.3.3.3 Mammals ................................ 68
4.3.4 Proteolytic cascades ............................ 71
4.3.5 The deployment of effectors ..................... 73
4.4 Immune defence protein families ........................ 73
4.4.1 Immunoglobulin-superfamily (IgSF) ............... 73
4.4.2 Leucine-rich repeats (LRRs) ..................... 73
4.4.2.1 Toll and Toll-like receptors (TLRs) .... 74
4.4.3 Lectins ......................................... 74
4.4.4 Other important families ........................ 74
4.4.4.1 Tumour necrosis factor family (TNF) .... 74
4.4.4.2 Cytokine receptor families ............. 75
4.4.4.3 Chemokine receptor family .............. 75
4.4.4.4 PGRP, GNBP ............................. 75
4.4.4.5 NOD and other intra-cellular sensors ... 75
4.4.4.6 Scavenger receptors (SRCR) ............. 75
4.4.4.7 Down syndrome cell adhesion molecules
(Dscam) ................................ 75
4.4.4.8 Fibrinogen-related protein (FREP) ...... 76
4.4.4.9 Variable domain chitin-binding
proteins (VCBPs) ....................... 76
4.4.4.10 Anti-microbial peptides (AMPs) ......... 76
4.5 The generation of diversity in recognition ............. 78
4.5.1 Polymorphism in the germ line ................... 78
4.5.2 Somatic generation of diversity ................. 80
4.5.2.1 Alternative splicing ................... 80
4.5.2.2 Somatic rearrangement, copy choice ..... 82
4.5.2.3 Somatic (hyper-) mutation, gene
conversion ............................. 82
4.5.3 The structure of immunoglobulins of В- and
T-cells ......................................... 83
4.5.3.1 B-cells ................................ 83
4.5.3.2 T-cells ................................ 87
4.6 The diversity of immune defences ....................... 88
4.6.1 Defence in prokaryotes .......................... 88
4.6.2 Defence in plants ............................... 88
4.6.3 Defence in invertebrates ........................ 89
4.6.3.1 Nematodes .............................. 89
4.6.3.2 Molluscs ............................... 89
4.6.3.3 Insects ................................ 89
4.6.3.4 Sea urchins ............................ 89
4.6.4 Early vertebrates ............................... 90
4.6.4.1 Cephalochordates ....................... 90
4.6.4.2 Urochordates (tunicates) ............... 90
4.6.4.3 Jawless vertebrates .................... 90
4.6.5 The jawed (higher) vertebrates .................. 90
4.7 Evolution of the immune system ......................... 94
4.7.1 Recognition of non-self ......................... 94
4.7.2 The evolution of adaptive immunity .............. 94
Summary ..................................................... 97
5 Ecological immunology ....................................... 98
5.1 Variation in parasitism ................................ 98
5.1.1 Variation in parasite load ...................... 98
5.1.2 Variation in susceptibility and immune
response ....................................... 102
5.2 Ecological immunology: the costs of defence ........... 105
5.2.1 General principles ............................. 105
5.2.2 Defence costs related to life history and
behaviour ...................................... 107
5.2.3 Cost of evolving immune defences ............... 109
5.2.3.1 Genetic costs associated with the
evolution of immune defences .......... 109
5.2.3.2 Physiological costs associated with
the evolution (maintenance) of immune
defences .............................. 110
5.2.4 Cost of using immune defences .................. 113
5.2.4.1 Genetic costs associated with the
deployment of immune defences ......... 113
5.2.4.2 Physiological costs associated with
the deployment of immune defences ..... 113
5.2.4.3 Costs due to self-reactivity .......... 116
5.3 The nature of defence costs ........................... 117
5.3.1 What is the limiting resource? ................. 118
5.3.1.1 Energy ................................ 118
5.3.1.2 Food and nutrients .................... 120
5.3.2 Regulation of allocation ....................... 121
5.3.2.1 Hormones as mediators ................. 121
5.4 'Immunocompetence' and the benefits of defence ........ 123
5.4.1 Correlating immune response and fitness ........ 123
5.4.2 Phenotype, immunocompetence, and fitness ....... 124
5.5 Strategies of immune defence .......................... 124
5.5.1 Optimal defence to increase recovery rate ...... 129
5.5.2 Specific vs. general defence ................... 130
5.5.3 Constitutive vs. induced defence ............... 130
5.5.4 Optimal memory ................................. 132
5.5.5 Robust defence ................................. 132
5.5.6 Optimal defence and host lifespan .............. 135
5.6 Tolerance as defence element .......................... 136
5.6.1 Measuring tolerance ............................ 137
5.6.2 The evolutionary consequences of tolerance ..... 139
Summary .................................................... 140
6 Parasites, immunity, and sexual selection .................. 141
6.1 Differences between the sexes ......................... 141
6.1.1 Males are generally more prone to parasites .... 141
6.1.2 The role of sex hormones in vertebrates ........ 144
6.2 Parasites and sexual selection ........................ 145
6.2.1 Female mate choice, immunity, and parasitism ... 147
6.2.2 Males indicate quality of resisting parasites .. 148
6.2.2.1 The Hamilton-Zuk hypothesis ........... 148
6.2.2.2 Symmetry as an indicator of male
quality ............................... 151
6.2.2.3 The immunocompetence handicap
hypothesis ............................ 152
6.2.2.4 Immunosuppression to avoid self-
damage ................................ 153
6.2.3 Male genotype and female self-reference ........ 155
6.2.3.1 Heterozygosity advantage .............. 155
6.2.3.2 Dissimilar genes ...................... 155
6.3 Sexual selection and immunity in invertebrates ........ 159
Summary .................................................... 164
7 Specificity ................................................ 165
7.1 Measuring specificity and host range .................. 165
7.1.1 List of observed hosts ......................... 165
7.1.2 Screening with genetic tools ................... 166
7.1.3 Experimental infections ........................ 166
7.2 Host-specificity of parasites ......................... 170
7.3 Evolution of the host range ........................... 170
7.3.1 Host range and ecological specialization ....... 170
7.3.2 Factors affecting host range ................... 173
7.3.2.1 Host range is limited by phylogenetic
constraints ........................... 173
7.3.2.2 Host range depends on the
phylogenetic age of the parasite
group ................................. 173
7.3.2.3 Host range depends on transmission
mode .................................. 173
7.3.2.4 Host range depends on the complexity
of the life-cycle ..................... 174
7.3.2.5 Host range depends on the stages of
the parasite's life-cycle ............. 174
7.3.2.6 Host range depends on the virulence
of the parasite ....................... 174
7.3.2.7 Host range depends on the variation
in host availability .................. 175
7.3.2.8 Host range depends on parasite
geographic distribution ............... 175
7.3.2.9 Host range depends on immune
defences .............................. 175
7.4 Specific defences of the host ......................... 177
7.4.1 Specificity beyond the immune system ........... 177
7.4.1.1 Behavioural defences .................. 177
7.4.1.2 Physical and chemical barriers ........ 177
7.4.2 Specificity of the adaptive immune system ...... 177
7.4.3 Specificity of the innate immune system ........ 179
7.5 Memory, immune priming, and trans-generational
transfer .............................................. 179
7.5.1 Individual immune memory ....................... 180
7.5.2 Trans-generational protection .................. 180
7.6 Adaptive diversity and cross-reactivity ............... 184
Summary .................................................... 186
8 Parasite immune evasion and manipulation of host
phenotype .................................................. 187
8.1 Parasites manipulate their hosts ...................... 187
8.2 The diversity of immune-evasion mechanisms ............ 190
8.2.1 Passive evasion ................................ 190
8.2.1.1 Hide away ............................. 190
8.2.1.2 Becoming 'invisible' .................. 190
8.2.1.3 Changing identity ..................... 190
8.2.1.4 Population escape by mutation ......... 190
8.2.1.5 Molecular mimicry ..................... 191
8.2.1.6 Quiescence ............................ 191
8.2.1.7 Capsule formation ..................... 191
8.2.2 Active evasion ................................. 191
8.2.3 Targets of immune evasion ...................... 193
8.2.3.1 Escape recognition .................... 196
8.2.3.2 Avoid complement attack ............... 196
8.2.3.3 Avoid being killed by
polymorphonuclear cells (PMNs) ........ 196
8.2.3.4 Avoid being killed by macrophages and
phagocytes ............................ 196
8.2.3.5 Manipulate the signalling network ..... 197
8.2.3.6 Interference with the antigen
presentation and processing pathways .. 197
8.2.3.7 Avoid being killed by the effectors ... 197
8.3 Manipulation of the host phenotype to increase
transmission .......................................... 198
8.3.1 Manipulation of host behaviour ................. 198
8.3.1.1 Site of transmission in space and
time .................................. 198
8.3.1.2 Transmission from host to vector ...... 203
8.3.1.3 Time of transmission .................. 203
8.3.2 Change of host morphology ...................... 204
8.3.3 Affecting transmission routes .................. 204
8.3.4 Affecting social behaviour ..................... 207
8.4 Manipulation of the host phenotype to increase
infection lifetime .................................... 207
8.4.1 Fecundity reduction ............................ 207
8.4.2 Changes of the social context .................. 209
8.5 Mechanisms of host phenotype manipulation ............. 210
8.6 Strategies of manipulation ............................ 213
8.6.1 What manipulation effort? ...................... 213
8.6.2 Multiple infections ............................ 214
8.7 Ecological significance of manipulation ............... 217
Summary .................................................... 217
9 Infection and pathogenesis ................................. 219
9.1 Infection and dose .................................... 219
9.1.1 Analysing infective dose ....................... 223
9.1.1.1 Individual effective dose (threshold
model) ................................ 223
9.1.1.2 Independent action model .............. 223
9.1.2 The manipulation hypothesis .................... 228
9.2 Similar parasites cause different pathologies ......... 229
9.2.1 The common cold ................................ 229
9.2.2 Influenza ...................................... 229
9.3 Pathogenesis: the mechanisms of virulence ............. 230
9.3.1 Impairing host capacities ...................... 232
9.3.2 Destruction of tissue .......................... 232
9.3.3 Virulence factors .............................. 232
9.3.3.1 Adhesion factors (adhesins) ........... 233
9.3.3.2 Colonization factors .................. 233
9.3.3.3 Invasion factors (invasins) ........... 233
9.3.3.4 Immune evasion factors ................ 233
9.3.3.5 Toxins ................................ 233
9.3.4 Toxins ......................................... 234
9.3.5 Proteases ...................................... 236
9.3.6 Pathogenesis by opportunistic infections ....... 237
9.4 Immunopathology ....................................... 237
9.4.1 Immunopathology associated with cytokines ...... 238
9.4.2 Immunopathology caused by immune-evasion
mechanisms ..................................... 238
9.5 The genetics of pathogenesis .......................... 241
Summary .................................................... 243
10 Host-parasite genetics ..................................... 244
10.1 The genetic architecture of host resistance ........... 244
10.1.1 Number and location of host resistance genes ... 244
10.1.1.1 QTL-mapping ........................... 244
10.1.1.2 Genomic sequences ..................... 245
10.1.1.3 Comparative genetic studies ........... 245
10.1.1.4 Resistance in plants and animals ...... 246
10.1.2 Genetics of parasite virulence ................. 250
10.1.2.1 Genetics of virulence in bacteria ..... 250
10.1.2.2 Example: genetics of virulence in
Salmonella ........................... 253
10.1.3 Variation in gene expression ................... 256
10.2 Evolutionary genetics of host-parasite interactions ... 259
10.2.1 Interaction between genotypes .................. 259
10.2.2 Models of genotypic interactions ............... 263
10.2.2.1 Gene-for-gene interaction (GFG) ....... 263
10.2.2.2 Matching specificities (matching
alleles) .............................. 266
10.2.3 Epistasis ...................................... 267
10.2.4 Inbreeding and heterozygosity .................. 268
10.2.4.1 Genetically variable populations ...... 268
10.2.4.2 Individual heterozygosity ............. 272
10.3 Signatures of selection ............................... 272
10.3.1 Selection drives populations genetically
apart .......................................... 274
10.3.1.1 Phytogeny of haplotypes ............... 274
10.3.1.2 Testing for genetic divergence ........ 274
10.3.2 Selection affects non-synonymous mutations ..... 275
10.3.3 Selective sweeps leave traces of linkage along
the genome ..................................... 275
10.4 Genetic structure of protozoan parasites .............. 276
Summary .................................................... 278
11 Epidemiology ............................................... 279
11.1 Population biology of host-parasitoid systems ......... 279
11.2 Epidemiology of infectious diseases: microparasites ... 282
11.2.1 TheSIR-model ................................... 285
11.2.2 Vaccination .................................... 288
11.2.3 Stochastic epidemiology ........................ 293
11.2.4 Spatial heterogeneity .......................... 295
11.3 Endemic infections and periodic outbreaks ............. 295
11.4 Epidemiology of vectored microparasites ............... 296
11.5 Epidemiology of macroparasites ........................ 297
11.5.1 The distribution of macroparasites among
hosts .......................................... 298
11.5.2 Population dynamics and models for
macroparasites ................................. 299
11.6 Immuno-epidemiology ................................... 299
11.6.1 Effects of immune response on parasites ........ 302
11.6.2 Effects of acquired immunity on
epidemiological patterns ....................... 303
11.6.3 Effects of immunity on population dynamics ..... 305
11.7 Epidemiology with evolutionary change ................. 305
11.8 Within-host epidemiology .............................. 307
11.8.1 Within-host dynamics of parasites .............. 308
11.8.2 Within-host competition between parasite
strains ........................................ 309
Summary .................................................... 311
12 Virulence .................................................. 312
12.1 Virulence ............................................. 312
12.1.1 Different meanings of virulence ................ 312
12.1.2 Virulence as a non-adaptive phenomenon ......... 312
12.1.2.1 Virulence as a side-effect ............ 313
12.1.2.2 Short-sighted evolution ............... 314
12.1.2.3 Virulence a negligible effect for the
parasite .............................. 315
12.1.3 Virulence as an evolved trait .................. 315
12.2 The evolution of virulence ............................ 319
12.2.1 Avirulence theory .............................. 319
12.2.2 Virulence as an adaptive trait ................. 319
12.3 Concepts of virulence evolution ....................... 322
12.3.1 Basic principles of evolutionary theory ........ 322
12.3.2 The recovery-virulence trade-off ............... 323
12.3.3 The transmission-virulence trade-off ........... 323
12.3.4 Horizontal vs. vertical transmission ........... 327
12.3.5 Host density and background mortality .......... 330
12.3.6 Host population size affected by parasitism .... 330
12.4 Within-host evolution ................................. 331
12.4.1 Within-host replication and clearance of the
infection ...................................... 331
12.4.2 Multiple infections ............................ 331
12.4.3 Kinship among co-infecting parasites ........... 334
12.4.4 Medical intervention and virulence ............. 339
12.4.5 Obligate killers ............................... 344
12.4.6 Immunopathology and virulence .................. 344
12.5 Life history of infection events ...................... 344
12.5.1 The timing of benefits and costs ............... 344
12.5.2 A generalized theory: the sensitivity
framework ...................................... 346
12.6 Within- vs. between-host selection .................... 348
12.7 Host population structure ............................. 350
12.7.1 Spatial structure .............................. 350
12.7.2 Variation in host types ........................ 350
12.7.3 Social structure ............................... 351
12.8 Non-equilibrium virulence ............................. 351
Summary .................................................... 352
13 Host-parasite (co-)evolution ............................... 354
13.1 Macro-evolution ....................................... 354
13.2 Micro-evolution ....................................... 359
13.2.1 Evolution of antibiotic resistance ............. 360
13.2.2 Costs of antibiotic resistance ................. 362
13.3 Micro-evolution: the maintenance of diversity ......... 364
13.3.1 Antagonistic host-parasite co-evolution ........ 364
13.3.2 Time-lagged negative frequency-dependent
selection ...................................... 365
13.3.3 Local adaptation ............................... 369
13.4 Antagonistic co-evolution, sex, and recombination ..... 374
13.4.1 Sexual reproduction ............................ 374
13.4.2 Meiotic recombination .......................... 374
13.5 The evolution of sex and recombination under
parasitism ............................................ 375
13.5.1 The evolution of sex ........................... 376
13.5.2 The evolution of meiotic recombination ......... 376
13.5.3 Empirical evidence: advantage for sex .......... 379
13.5.4 Empirical evidence: advantage for
recombination .................................. 383
13.6 Selective sweeps ...................................... 386
Summary .................................................... 389
14 Ecology .................................................... 390
14.1 Parasites and host life-history ....................... 390
14.1.1 Changes in reproductive patterns ............... 390
14.1.2 Gigantism ...................................... 391
14.1.3 Group living ................................... 393
14.2 Host populations ...................................... 395
14.2.1 Population regulation by parasites ............. 397
14.2.2 Population decline and extinction .............. 399
14.3 Host ecological communities ........................... 401
14.3.1 Parasite effects on host competition ........... 401
14.3.2 Communities of hosts ........................... 401
14.3.3 Food webs ...................................... 405
14.4 Parasite ecology ...................................... 406
14.4.1 Geographical patterns .......................... 406
14.4.1.1 Species-area relationship ............. 406
14.4.1.2 Species-isolation relationship ........ 406
14.4.1.3 Latitudinal gradients ................. 407
14.4.2 Parasite community assembly .................... 409
14.5 Invasions ............................................. 410
14.5.1 Host invasions ................................. 410
14.5.1.1 Escape from parasites ................ 411
14.5.1.2 Characteristics of parasites .......... 411
14.5.2 Invasion by parasites (disease emergence) ...... 411
14.5.2.1 Biological processes .................. 411
14.5.2.2 Abiotic correlates of parasite
invasion success ...................... 413
74.5.2.1 Global patterns ....................... 413
14.5.3 Climate change and disease emergence ........... 414
Summary .................................................... 415
Glossary ...................................................... 417
List of Immunological Acronyms ................................ 429
References .................................................... 435
Subject Index ................................................. 499
Taxonomic Index ............................................... 506
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