| Preface |
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xvii | |
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1 | (8) |
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1 | (2) |
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1.2 Some lessons provided by yellow fever |
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3 | (3) |
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1.2.1 The parasite life-cycle can be complex |
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4 | (1) |
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1.2.2 Not all host and parasite strains are the same |
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4 | (1) |
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1.2.3 Complex physiological and molecular mechanisms underlie the infection |
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4 | (1) |
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1.2.4 Parasites and hosts are populations |
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5 | (1) |
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1.2.5 Parasites can be controlled when we understand them |
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5 | (1) |
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1.3 Parasites in our times |
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6 | (3) |
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8 | (1) |
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2 The study of evolutionary parasitology |
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9 | (9) |
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2.1 The evolutionary process |
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9 | (3) |
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2.2 Questions about host-parasite interactions |
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12 | (1) |
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2.3 Selection and units that evolve |
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13 | (1) |
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14 | (1) |
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2.5 Studying adaptation: optimality and evolutionarily stable strategies (ESS) |
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14 | (2) |
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15 | (1) |
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2.5.2 Evolutionarily stable strategies (ESS) |
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16 | (1) |
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16 | (2) |
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17 | (1) |
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3 The diversity and natural history of parasites |
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18 | (34) |
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3.1 The ubiquity of parasites |
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18 | (2) |
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3.2 A systematic overview of parasites |
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20 | (13) |
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20 | (1) |
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21 | (1) |
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22 | (1) |
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22 | (2) |
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3.2.3 The basal Eukaryotes |
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24 | (1) |
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24 | (1) |
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25 | (1) |
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25 | (1) |
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26 | (1) |
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26 | (1) |
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27 | (1) |
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3.2.6 Nematodes (roundworms) |
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28 | (1) |
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29 | (1) |
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30 | (1) |
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30 | (1) |
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31 | (1) |
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31 | (1) |
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31 | (1) |
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31 | (1) |
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3.2.10.4 Branchiura (fish lice) |
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31 | (1) |
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31 | (1) |
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3.2.11 Mites (Acari), ticks, lice (Mallophaga, Anoplura) |
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32 | (1) |
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3.2.12 Parasitic insects (parasitoids) |
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33 | (1) |
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3.3 The evolution of parasitism |
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33 | (5) |
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3.3.1 Evolution of parasitism in nematodes |
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34 | (1) |
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3.3.2 Evolution of parasitism in trypanosomes |
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35 | (3) |
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3.4 The diversity and evolution of parasite life-cycles |
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38 | (14) |
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3.4.1 Steps in a parasite's life-cycle |
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38 | (1) |
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3.4.1.1 Step 1: finding a host |
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38 | (1) |
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3.4.1.1.1 Passive dispersion |
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38 | (1) |
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3.4.1.1.2 Active host-finding |
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39 | (1) |
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3.4.1.2 Step 2: infecting and establishment in the host |
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39 | (1) |
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3.4.1.3 Step 3: growth, multiplication |
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39 | (1) |
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3.4.1.4 Step 4: reproduction |
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40 | (1) |
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3.4.1.5 Step 5: transmission |
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40 | (1) |
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3.4.2 Modes of transmission |
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40 | (1) |
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3.4.2.1 Direct transmission |
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40 | (1) |
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3.4.2.2 Transmission with paratenic hosts |
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40 | (2) |
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3.4.2.3 Vector transmission |
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42 | (1) |
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3.4.3 Trematode life-cycles |
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42 | (4) |
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3.4.4 The evolution of complex parasite life-cycles |
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46 | (5) |
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51 | (1) |
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4 The natural history of defences |
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52 | (46) |
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52 | (7) |
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4.1.1 Pre-infection defences |
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52 | (1) |
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4.1.1.1 Spatial avoidance |
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52 | (1) |
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4.1.1.2 Temporal avoidance |
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53 | (1) |
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4.1.1.3 Avoiding certain diets |
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53 | (2) |
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55 | (1) |
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4.1.1.5 Mating behaviour and mate choice |
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55 | (1) |
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55 | (1) |
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4.1.1.7 Anticipatory defences |
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55 | (1) |
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55 | (1) |
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4.1.2 Post-infection defences |
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55 | (1) |
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4.1.2.1 Behavioural changes |
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56 | (1) |
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56 | (1) |
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4.1.2.3 Fever and chilling |
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57 | (1) |
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57 | (2) |
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4.2 Defence by the immune system |
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59 | (1) |
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4.3 Basic elements of the immune defence |
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60 | (13) |
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4.3.1 Humoral and cellular defences |
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60 | (2) |
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62 | (2) |
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4.3.1.2 Melanization, encapsulation |
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64 | (1) |
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4.3.1.3 Clotting, nodule formation |
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64 | (1) |
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65 | (1) |
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4.3.2 Innate and adaptive (acquired) immunity |
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65 | (1) |
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4.3.2.1 Innate immune defence |
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65 | (1) |
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4.3.2.2 Adaptive (acquired) immunity |
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65 | (1) |
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4.3.3 Signalling cascades |
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66 | (2) |
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68 | (1) |
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68 | (1) |
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68 | (3) |
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4.3.4 Proteolytic cascades |
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71 | (2) |
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4.3.5 The deployment of effectors |
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73 | (1) |
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4.4 Immune defence protein families |
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73 | (5) |
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4.4.1 Immunoglobulin-superfamily(lgSF) |
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73 | (1) |
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4.4.2 Leucine-rich repeats (LRRs) |
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73 | (1) |
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4.4.2.1 Toll and Toll-like receptors (TLRs) |
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74 | (1) |
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74 | (1) |
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4.4.4 Other important families |
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74 | (1) |
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4.4.4.1 Tumour necrosis factor family (TNF) |
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74 | (1) |
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4.4.4.2 Cytokine receptor families |
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75 | (1) |
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4.4.4.3 Chemokine receptor family |
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75 | (1) |
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75 | (1) |
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4.4.4.5 NOD and other intra-cellular sensors |
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75 | (1) |
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4.4.4.6 Scavenger receptors (SRCR) |
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75 | (1) |
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4.4.4.7 Down syndrome cell adhesion molecules (Dscam) |
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75 | (1) |
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4.4.4.8 Fibrinogen-related protein (FREP) |
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76 | (1) |
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4.4.4.9 Variable domain chitin-binding proteins (VCBPs) |
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76 | (1) |
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4.4.4.10 Anti-microbial peptides (AMPs) |
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76 | (2) |
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4.5 The generation of diversity in recognition |
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78 | (10) |
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4.5.1 Polymorphism in the germ line |
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78 | (2) |
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4.5.2 Somatic generation of diversity |
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80 | (1) |
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4.5.2.1 Alternative splicing |
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80 | (2) |
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4.5.2.2 Somatic rearrangement, copy choice |
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82 | (1) |
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4.5.2.3 Somatic (hyper-) mutation, gene conversion |
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82 | (1) |
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4.5.3 The structure of immunoglobulins of B-and T-cells |
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83 | (1) |
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83 | (4) |
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87 | (1) |
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4.6 The diversity of immune defences |
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88 | (6) |
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4.6.1 Defence in prokaryotes |
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88 | (1) |
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88 | (1) |
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4.6.3 Defence in invertebrates |
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89 | (1) |
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89 | (1) |
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89 | (1) |
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89 | (1) |
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89 | (1) |
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90 | (1) |
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90 | (1) |
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4.6.4.2 Urochordates (tunicates) |
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90 | (1) |
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4.6.4.3 Jawless vertebrates |
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90 | (1) |
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4.6.5 The jawed (higher) vertebrates |
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90 | (4) |
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4.7 Evolution of the immune system |
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94 | (4) |
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4.7.1 Recognition of non-self |
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94 | (1) |
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4.7.2 The evolution of adaptive immunity |
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94 | (3) |
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97 | (1) |
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98 | (43) |
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5.1 Variation in parasitism |
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98 | (7) |
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5.1.1 Variation in parasite load |
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98 | (4) |
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5.1.2 Variation in susceptibility and immune response |
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102 | (3) |
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5.2 Ecological immunology: the costs of defence |
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105 | (12) |
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105 | (2) |
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5.2.2 Defence costs related to life history and behaviour |
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107 | (2) |
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5.2.3 Cost of evolving immune defences |
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109 | (1) |
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5.2.3.1 Genetic costs associated with the evolution of immune defences |
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109 | (1) |
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5.2.3.2 Physiological costs associated with the evolution (maintenance) of immune defences |
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110 | (3) |
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5.2.4 Cost of using immune defences |
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113 | (1) |
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5.2.4.1 Genetic costs associated with the deployment of immune defences |
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113 | (1) |
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5.2.4.2 Physiological costs associated with the deployment of immune defences |
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113 | (3) |
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5.2.4.3 Costs due to self-reactivity |
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116 | (1) |
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5.3 The nature of defence costs |
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117 | (6) |
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5.3.1 What is the limiting resource? |
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118 | (1) |
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118 | (2) |
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5.3.1.2 Food and nutrients |
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120 | (1) |
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5.3.2 Regulation of allocation |
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121 | (1) |
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5.3.2.1 Hormones as mediators |
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121 | (2) |
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5.4 `Immunocompetence' and the benefits of defence |
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123 | (1) |
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5.4.1 Correlating immune response and fitness |
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123 | (1) |
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5.4.2 Phenotype, immunocompetence, and fitness |
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124 | (1) |
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5.5 Strategies of immune defence |
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124 | (12) |
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5.5.1 Optimal defence to increase recovery rate |
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129 | (1) |
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5.5.2 Specific vs. general defence |
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130 | (1) |
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5.5.3 Constitutive vs. induced defence |
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130 | (2) |
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132 | (1) |
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132 | (3) |
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5.5.6 Optimal defence and host lifespan |
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135 | (1) |
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5.6 Tolerance as defence element |
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136 | (5) |
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5.6.1 Measuring tolerance |
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137 | (2) |
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5.6.2 The evolutionary consequences of tolerance |
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139 | (1) |
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140 | (1) |
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6 Parasites, immunity, and sexual selection |
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141 | (24) |
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6.1 Differences between the sexes |
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141 | (4) |
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6.1.1 Males are generally more prone to parasites |
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141 | (3) |
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6.1.2 The role of sex hormones in vertebrates |
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144 | (1) |
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6.2 Parasites and sexual selection |
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145 | (14) |
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6.2.1 Female mate choice, immunity, and parasitism |
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147 | (1) |
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6.2.2 Males indicate quality of resisting parasites |
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148 | (1) |
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6.2.2.1 The Hamilton--Zuk hypothesis |
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148 | (3) |
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6.2.2.2 Symmetry as an indicator of male quality |
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151 | (1) |
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6.2.2.3 The immunocompetence handicap hypothesis |
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152 | (1) |
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6.2.2.4 Immunosuppression to avoid self-damage |
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153 | (2) |
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6.2.3 Male genotype and female self-reference |
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155 | (1) |
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6.2.3.1 Heterozygosity advantage |
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155 | (1) |
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155 | (4) |
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6.3 Sexual selection and immunity in invertebrates |
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159 | (6) |
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164 | (1) |
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165 | (22) |
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7.1 Measuring specificity and host range |
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165 | (5) |
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7.1.1 List of observed hosts |
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165 | (1) |
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7.1.2 Screening with genetic tools |
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166 | (1) |
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7.1.3 Experimental infections |
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166 | (4) |
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7.2 Host-specificity of parasites |
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170 | (1) |
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7.3 Evolution of the host range |
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170 | (7) |
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7.3.1 Host range and ecological specialization |
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170 | (3) |
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7.3.2 Factors affecting host range |
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173 | (1) |
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7.3.2.1 Host range is limited by phylogenetic constraints |
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173 | (1) |
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7.3.2.2 Host range depends on the phylogenetic age of the parasite group |
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173 | (1) |
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7.3.2.3 Host range depends on transmission mode |
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173 | (1) |
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7.3.2.4 Host range depends on the complexity of the life-cycle |
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174 | (1) |
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7.3.2.5 Host range depends on the stages of the parasite's life-cycle |
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174 | (1) |
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7.3.2.6 Host range depends on the virulence of the parasite |
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174 | (1) |
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7.3.2.7 Host range depends on the variation in host availability |
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175 | (1) |
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7.3.2.8 Host range depends on parasite geographic distribution |
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175 | (1) |
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7.3.2.9 Host range depends on immune defences |
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175 | (2) |
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7.4 Specific defences of the host |
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177 | (2) |
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7.4.1 Specificity beyond the immune system |
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177 | (1) |
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7.4.1.1 Behavioural defences |
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177 | (1) |
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7.4.1.2 Physical and chemical barriers |
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177 | (1) |
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7.4.2 Specificity of the adaptive immune system |
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177 | (2) |
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7.4.3 Specificity of the innate immune system |
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179 | (1) |
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7.5 Memory, immune priming, and trans-generational transfer |
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179 | (5) |
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7.5.1 Individual immune memory |
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180 | (1) |
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7.5.2 Trans-generational protection |
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180 | (4) |
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7.6 Adaptive diversity and cross-reactivity |
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184 | (3) |
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186 | (1) |
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8 Parasite immune evasion and manipulation of host phenotype |
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187 | (32) |
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8.1 Parasites manipulate their hosts |
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187 | (3) |
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8.2 The diversity of immune-evasion mechanisms |
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190 | (8) |
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190 | (1) |
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190 | (1) |
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8.2.1.2 Becoming `invisible' |
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190 | (1) |
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8.2.1.3 Changing identity |
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190 | (1) |
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8.2.1.4 Population escape by mutation |
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190 | (1) |
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8.2.1.5 Molecular mimicry |
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191 | (1) |
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191 | (1) |
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8.2.1.7 Capsule formation |
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191 | (1) |
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191 | (2) |
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8.2.3 Targets of immune evasion |
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193 | (3) |
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8.2.3.1 Escape recognition |
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196 | (1) |
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8.2.3.2 Avoid complement attack |
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196 | (1) |
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8.2.3.3 Avoid being killed by polymorphonuclear cells (PMNs) |
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196 | (1) |
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8.2.3.4 Avoid being killed by macrophages and phagocytes |
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196 | (1) |
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8.2.3.5 Manipulate the signalling network |
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197 | (1) |
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8.2.3.6 Interference with the antigen presentation and processing pathways |
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197 | (1) |
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8.2.3.7 Avoid being killed by the effectors |
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197 | (1) |
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8.3 Manipulation of the host phenotype to increase transmission |
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198 | (9) |
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8.3.1 Manipulation of host behaviour |
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198 | (1) |
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8.3.1.1 Site of transmission in space and time |
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198 | (5) |
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8.3.1.2 Transmission from host to vector |
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203 | (1) |
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8.3.1.3 Time of transmission |
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203 | (1) |
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8.3.2 Change of host morphology |
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204 | (1) |
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8.3.3 Affecting transmission routes |
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204 | (3) |
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8.3.4 Affecting social behaviour |
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207 | (1) |
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8.4 Manipulation of the host phenotype to increase infection lifetime |
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207 | (3) |
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8.4.1 Fecundity reduction |
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207 | (2) |
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8.4.2 Changes of the social context |
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209 | (1) |
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8.5 Mechanisms of host phenotype manipulation |
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210 | (3) |
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8.6 Strategies of manipulation |
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213 | (4) |
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8.6.1 What manipulation effort? |
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213 | (1) |
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8.6.2 Multiple infections |
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214 | (3) |
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8.7 Ecological significance of manipulation |
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217 | (2) |
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217 | (2) |
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9 Infection and pathogenesis |
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219 | (25) |
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219 | (10) |
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9.1.1 Analysing infective dose |
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223 | (1) |
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9.1.1.1 Individual effective dose (threshold model) |
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223 | (1) |
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9.1.1.2 Independent action model |
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223 | (5) |
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9.1.2 The manipulation hypothesis |
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228 | (1) |
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9.2 Similar parasites cause different pathologies |
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229 | (1) |
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229 | (1) |
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229 | (1) |
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9.3 Pathogenesis: the mechanisms of virulence |
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230 | (7) |
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9.3.1 Impairing host capacities |
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232 | (1) |
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9.3.2 Destruction of tissue |
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232 | (1) |
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232 | (1) |
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9.3.3.1 Adhesion factors (adhesins) |
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233 | (1) |
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9.3.3.2 Colonization factors |
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233 | (1) |
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9.3.3.3 Invasion factors (invasins) |
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233 | (1) |
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9.3.3.4 Immune evasion factors |
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233 | (1) |
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233 | (1) |
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234 | (2) |
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236 | (1) |
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9.3.6 Pathogenesis by opportunistic infections |
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237 | (1) |
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237 | (4) |
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9.4.1 Immunopathology associated with cytokines |
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238 | (1) |
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9.4.2 Immunopathology caused by immune-evasion mechanisms |
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238 | (3) |
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9.5 The genetics of pathogenesis |
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241 | (3) |
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243 | (1) |
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10 Host-parasite genetics |
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244 | (35) |
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10.1 The genetic architecture of host resistance |
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244 | (15) |
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10.1.1 Number and location of host resistance genes |
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244 | (1) |
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244 | (1) |
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10.1.1.2 Genomic sequences |
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245 | (1) |
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10.1.1.3 Comparative genetic studies |
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245 | (1) |
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10.1.1.4 Resistance in plants and animals |
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246 | (4) |
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10.1.2 Genetics of parasite virulence |
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250 | (1) |
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10.1.2.1 Genetics of virulence in bacteria |
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250 | (3) |
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10.1.2.2 Example: genetics of virulence in Salmonella |
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253 | (3) |
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10.1.3 Variation in gene expression |
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256 | (3) |
|
10.2 Evolutionary genetics of host-parasite interactions |
|
|
259 | (13) |
|
10.2.1 Interaction between genotypes |
|
|
259 | (4) |
|
10.2.2 Models of genotypic interactions |
|
|
263 | (1) |
|
10.2.2.1 Gene-for-gene interaction (GFG) |
|
|
263 | (3) |
|
10.2.2.2 Matching specificities (matching alleles) |
|
|
266 | (1) |
|
|
|
267 | (1) |
|
10.2.4 Inbreeding and heterozygosity |
|
|
268 | (1) |
|
10.2.4.1 Genetically variable populations |
|
|
268 | (4) |
|
10.2.4.2 Individual heterozygosity |
|
|
272 | (1) |
|
10.3 Signatures of selection |
|
|
272 | (4) |
|
10.3.1 Selection drives populations genetically apart |
|
|
274 | (1) |
|
10.3.1.1 Phylogeny of haplotypes |
|
|
274 | (1) |
|
10.3.1.2 Testing for genetic divergence |
|
|
274 | (1) |
|
10.3.2 Selection affects non-synonymous mutations |
|
|
275 | (1) |
|
10.3.3 Selective sweeps leave traces of linkage along the genome |
|
|
275 | (1) |
|
10.4 Genetic structure of protozoan parasites |
|
|
276 | (3) |
|
|
|
278 | (1) |
|
|
|
279 | (33) |
|
11.1 Population biology of host-parasitoid systems |
|
|
279 | (3) |
|
11.2 Epidemiology of infectious diseases: microparasites |
|
|
282 | (13) |
|
|
|
285 | (3) |
|
|
|
288 | (5) |
|
11.2.3 Stochastic epidemiology |
|
|
293 | (2) |
|
11.2.4 Spatial heterogeneity |
|
|
295 | (1) |
|
11.3 Endemic infections and periodic outbreaks |
|
|
295 | (1) |
|
11.4 Epidemiology of vectored microparasites |
|
|
296 | (1) |
|
11.5 Epidemiology of macroparasites |
|
|
297 | (2) |
|
11.5.1 The distribution of macroparasites among hosts |
|
|
298 | (1) |
|
11.5.2 Population dynamics and models for macroparasites |
|
|
299 | (1) |
|
|
|
299 | (6) |
|
11.6.1 Effects of immune response on parasites |
|
|
302 | (1) |
|
11.6.2 Effects of acquired immunity on epidemiological patterns |
|
|
303 | (2) |
|
11.6.3 Effects of immunity on population dynamics |
|
|
305 | (1) |
|
11.7 Epidemiology with evolutionary change |
|
|
305 | (2) |
|
11.8 Within-host epidemiology |
|
|
307 | (5) |
|
11.8.1 Within-host dynamics of parasites |
|
|
308 | (1) |
|
11.8.2 Within-host competition between parasite strains |
|
|
309 | (2) |
|
|
|
311 | (1) |
|
|
|
312 | (42) |
|
|
|
312 | (7) |
|
12.1.1 Different meanings of virulence |
|
|
312 | (1) |
|
12.1.2 Virulence as a non-adaptive phenomenon |
|
|
312 | (1) |
|
12.1.2.1 Virulence as a side-effect |
|
|
313 | (1) |
|
12.1.2.2 Short-sighted evolution |
|
|
314 | (1) |
|
12.1.2.3 Virulence a negligible effect for the parasite |
|
|
315 | (1) |
|
12.1.3 Virulence as an evolved trait |
|
|
315 | (4) |
|
12.2 The evolution of virulence |
|
|
319 | (3) |
|
|
|
319 | (1) |
|
12.2.2 Virulence as an adaptive trait |
|
|
319 | (3) |
|
12.3 Concepts of virulence evolution |
|
|
322 | (9) |
|
12.3.1 Basic principles of evolutionary theory |
|
|
322 | (1) |
|
12.3.2 The recovery-virulence trade-off |
|
|
323 | (1) |
|
12.3.3 The transmission-virulence trade-off |
|
|
323 | (4) |
|
12.3.4 Horizontal vs. vertical transmission |
|
|
327 | (3) |
|
12.3.5 Host density and background mortality |
|
|
330 | (1) |
|
12.3.6 Host population size affected by parasitism |
|
|
330 | (1) |
|
12.4 Within-host evolution |
|
|
331 | (13) |
|
12.4.1 Within-host replication and clearance of the infection |
|
|
331 | (1) |
|
12.4.2 Multiple infections |
|
|
331 | (3) |
|
12.4.3 Kinship among co-infecting parasites |
|
|
334 | (5) |
|
12.4.4 Medical intervention and virulence |
|
|
339 | (5) |
|
|
|
344 | (1) |
|
12.4.6 Immunopathology and virulence |
|
|
344 | (1) |
|
12.5 Life history of infection events |
|
|
344 | (4) |
|
12.5.1 The timing of benefits and costs |
|
|
344 | (2) |
|
12.5.2 A generalized theory: the sensitivity framework |
|
|
346 | (2) |
|
12.6 Within- vs. between-host selection |
|
|
348 | (2) |
|
12.7 Host population structure |
|
|
350 | (1) |
|
|
|
350 | (1) |
|
12.7.2 Variation in host types |
|
|
350 | (1) |
|
|
|
351 | (1) |
|
12.8 Non-equilibrium virulence |
|
|
351 | (3) |
|
|
|
352 | (2) |
|
13 Host-parasite (co-)evolution |
|
|
354 | (36) |
|
|
|
354 | (5) |
|
|
|
359 | (5) |
|
13.2.1 Evolution of antibiotic resistance |
|
|
360 | (2) |
|
13.2.2 Costs of antibiotic resistance |
|
|
362 | (2) |
|
13.3 Micro-evolution: the maintenance of diversity |
|
|
364 | (10) |
|
13.3.1 Antagonistic host-parasite co-evolution |
|
|
364 | (1) |
|
13.3.2 Time-lagged negative frequency-dependent selection |
|
|
365 | (4) |
|
|
|
369 | (5) |
|
13.4 Antagonistic co-evolution, sex, and recombination |
|
|
374 | (1) |
|
13.4.1 Sexual reproduction |
|
|
374 | (1) |
|
13.4.2 Meiotic recombination |
|
|
374 | (1) |
|
13.5 The evolution of sex and recombination under parasitism |
|
|
375 | (11) |
|
13.5.1 The evolution of sex |
|
|
376 | (1) |
|
13.5.2 The evolution of meiotic recombination |
|
|
376 | (3) |
|
13.5.3 Empirical evidence: advantage for sex |
|
|
379 | (4) |
|
13.5.4 Empirical evidence: advantage for recombination |
|
|
383 | (3) |
|
|
|
386 | (4) |
|
|
|
389 | (1) |
|
|
|
390 | (27) |
|
14.1 Parasites and host life-history |
|
|
390 | (5) |
|
14.1.1 Changes in reproductive patterns |
|
|
390 | (1) |
|
|
|
391 | (2) |
|
|
|
393 | (2) |
|
|
|
395 | (6) |
|
14.2.1 Population regulation by parasites |
|
|
397 | (2) |
|
14.2.2 Population decline and extinction |
|
|
399 | (2) |
|
14.3 Host ecological communities |
|
|
401 | (5) |
|
14.3.1 Parasite effects on host competition |
|
|
401 | (1) |
|
14.3.2 Communities of hosts |
|
|
401 | (4) |
|
|
|
405 | (1) |
|
|
|
406 | (4) |
|
14.4.1 Geographical patterns |
|
|
406 | (1) |
|
14.4.1.1 Species-area relationship |
|
|
406 | (1) |
|
14.4.1.2 Species-isolation relationship |
|
|
406 | (1) |
|
14.4.1.3 Latitudinal gradients |
|
|
407 | (2) |
|
14.4.2 Parasite community assembly |
|
|
409 | (1) |
|
|
|
410 | (7) |
|
|
|
410 | (1) |
|
14.5.1.1 Escape from parasites |
|
|
411 | (1) |
|
14.5.1.2 Characteristics of parasites |
|
|
411 | (1) |
|
14.5.2 Invasion by parasites (disease emergence) |
|
|
411 | (1) |
|
14.5.2.1 Biological processes |
|
|
411 | (2) |
|
14.5.2.2 Abiotic correlates of parasite invasion success |
|
|
413 | (1) |
|
|
|
413 | (1) |
|
14.5.3 Climate change and disease emergence |
|
|
414 | (1) |
|
|
|
415 | (2) |
| Glossary |
|
417 | (12) |
| List of Immunological Acronyms |
|
429 | (6) |
| References |
|
435 | (64) |
| Subject Index |
|
499 | (7) |
| Taxonomic Index |
|
506 | |