Table Of ContentOUP CORRECTED PROOF – FINAL, 13/06/21, SPi
Evolutionary Parasitology
OUP CORRECTED PROOF – FINAL, 13/06/21, SPi
OUP CORRECTED PROOF – FINAL, 13/06/21, SPi
Evolutionary
Parasitology
The Integrated Study of Infections,
Immunology, Ecology, and Genetics
Second Edition
Paul Schmid- Hempel
Emeritus Professor, Institute of Integrative Biology (IBZ) and Genetic Diversity Centre,
ETH Zürich, Switzerland
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1
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Preface
Parasites and infectious diseases are everywhere parasites have evolved mind-b oggling mechanisms
around us and have affected the ecology and evolu- and strategies to evade, overwhelm, and manipu-
tion of organisms since the early days of life on this late their hosts in their own favour—this is even
planet. In fact, this second edition of Evolutionary true for viruses that undermine their hosts’ defence
Parasitology was finished during the Corona year, 2020. systems in amazing ways. Therefore, to unravel
The pandemic brought grief and misery to many these fantastic processes and to clarify the evolu-
people, not to speak of the enormous economic costs. tionary reasons for the enormous diversity of host
At the same time, this pandemic is an impressive defences and parasite strategies is an endlessly cap-
illustration of the pervasive influence of parasitism tivating venture.
that affects virtually all aspects of the hosts’ lives. This is a completely rewritten update of Evolu-
The field of evolutionary parasitology, therefore, cuts tionary Parasitology. It contains a number of tables
across many disciplines for a more comprehensive that cannot be a comprehensive review of the
approach to studying hosts and parasites, to appreci- re spect ive topics. Such an attempt would be close to
ate the mechanisms that guide their interactions and impossible, given the enormous range of activities
to identify the selective forces that shape their biology. in this huge area. Rather, and as in the previous edi-
As before, I am using the generic term ‘parasite’ tion, the tables should illustrate typical studies,
to cover various other names, such as ‘pathogen’ or while giving an impression of the variety of study
‘parasitoid’, which are more common in fields like subjects and approaches. As before, I must also
medicine or agriculture. However, parasitism is the apologize to the plant world that my examples
core ecological relationship towards which all sci- are primarily zoonotic in origin. Similarly, social
entific endeavours in the larger field gravitate. This parasites such as inquiline ants or brood para-
relationship is based on molecular and physiol ogic al sites in birds are not considered in much detail.
processes, on probabilities of contacts, on binding Nevertheless, the principles guiding those host–
between surfaces and specific molecules, but also parasite interactions are also the topics of this book.
results in more or less success of either party. Looking back, it is astonishing to see how much
Hence, the relationship is also under selection and has happened in the broader field within the decade
has evolved and co-e volved over the aeons and still since the original book appeared. Three elements
continues to do so. In some cases, we see fast evolu- contributed in important ways. Firstly, the advance
tionary changes, as with the rise of antib iot ic resist- in molecular technologies is breathtaking. What once
ance in bacteria, whereas the conserved nature of used weeks, is now done in a day, and at a fraction
some elements in immune defence systems points of the cost. Sequencing technologies, for example,
to their deep ancestry across organisms. Indeed, have sparked a new age for virology, allowing an
immune systems are among the most complex nat- ongoing epidemic to be traced almost in real time.
ural systems that have evolved and, doubtlessly, Discoveries based on mechanisms in immune defence
parasitism was a major driver along this way. But systems, such as RNAi or CRISPR–Cas, allow the
parasites are not just the passive partners, as their geno types of organisms to be changed in unprece-
typical organismal simplicity would suggest. Instead, dented ways. And with mRNA technology a next
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vi PREFACE
toolbox is already on the horizon that not only ting over the years; the interactions with the groups
makes for a new generation of vaccines but can help of Sebastian Bonhoeffer and Roland Regoes espe-
to further dissect the mechanisms underlying host– cially helped me to reach out into the theoretical
parasite interactions. A second methodical element domains. Moreover, good fortune has brought many
that has contributed to the advance in the field is outstanding students and postdocs to my own
the progress in mathematical algorithms and com- research group. Working together on topics of host–
puting power, often lumped together as bioinfor- parasite interactions has been enriching, and a real
matics, that makes it possible to use large amounts pleasure. From the more recent past, I just mention
of information and to analyse these with improved Boris Baer, Seth Barribeau, Mark Brown, Jukka
statistical techniques. Reconstructing the molecular Jokela, Hauke Koch, Joachim Kurtz, Yannick Moret,
epidemiology of viral diseases is just one of the Kathrin Näpflin, Oliver Otti, Livia Roth, Ben Sadd,
applications of these powerf ul methods. Finally, the Rahel Salathé, Yuko Ulrich, Maze Wegner, Lena
field has progressed in its concepts, which is the Wilfert, without any disregard for all the others that
ultimate aim of any scientific exploration. For have contributed in many other ways. The adminis-
instance, the early phases of infection have come trative and technical help of Rita Jenny, Roland
into focus, as did concepts to predict the outcome of Loosli, Christine Reber from IBZ, and Aria Minder
an infection based on measures of host status at cer- from the Genetic Diversity Centre kept many a bur-
tain stages of the process. Clearly, evolutionary den off my table. Of course, my wife Regula has not
parasitology has matured, but it will not end soon— only shared the ups and downs during writing, but
too diverse and intriguing are its subjects, too rivet- has also helped in many and im port ant ways, both
ing the study of these, and too important the scientifically and with technical support. Finally, a
practical implications for matters of agriculture, number of colleagues have volunteered to read
conservation biology, medicine, and public health. through the earlier drafts. I am thus very grateful
The daily work of a scientist often is a very lone- for the valuable input given by Seth Barribeau,
some activity, but the process of doing science is Mark Brown, Austin Calhoun, Roger Kouyos, Elyse
not. Therefore, this book also rests on the work of McCormick, Andrew Read, Roland Regoes, Bryan
many others. I have been blessed to meet so many Sierra Rivera, Jens Rolff, Ben Sadd, and Logan
outstanding colleagues and to have the chance to Sauers. A special thanks goes to Louis du Pasquier
discuss questions at the forefront of their respective who had already helped with the first edition, and
fields, all of which has influenced this book perhaps whose critical advice was essential for the discus-
more than is visible. To pick just a few, I am grateful sion of immune defences. The remaining errors are,
for the extended contacts with Janis Antonovics, Mike of course, mine. Last but not least, I thank Ian
Boots, Sylvia Cremer, Dieter Ebert, Steve Frank, Sherman and Charles Bath from Oxford University
Andrea Graham, Andrew Read, Jens Rolff, David Press for their generous support and unobtrusive
Schneider, and many others. David Schneider’s coverage of the entire process. May the efforts aid
concept of the disease space has been a particularly the field of evolutionary parasitology and advance
illuminating addition and is used in this book as a our scientific understanding of nature.
guide through the different sections—in the hope
that it will always show the relationship between Paul Schmid- Hempel
the underlying mechanisms and the ecologic and November 2020
evolutionary outcome of a parasitic infection. My ETH Zürich, Institute of
own scientific home in the Institute of Integrative Integrative Biology (IBZ), and
Biology (IBZ) has been an enormously fruitful set- Genetic Diversity Centre at ETH, Switzerland
OUP CORRECTED PROOF – FINAL, 13/06/21, SPi
Contents
Preface v
List of common acronyms xix
Glossary xxiii
1 Parasites and their significance 1
1.1 The Panama Canal 1
1.2 Some lessons provided by yellow fever 3
1.2.1 Parasites have different life cycles and transmission modes 3
1.2.2 Not all host individuals, and not all parasite strains, are the same 5
1.2.3 Physiological and molecular mechanisms underlie the infection 5
1.2.4 Parasites and hosts are populations 6
1.2.5 Parasites can be controlled when we understand them 6
1.3 Parasites are not a threat of the past 6
2 The study of evolutionary parasitology 9
2.1 The evolutionary process 9
2.2 Questions in evolutionary biology 12
2.3 Selection and units that evolve 12
2.4 Life history 15
2.5 Studying adaptation 16
2.5.1 Optimality 16
2.5.2 Evolutionarily stable strategies (ESS) 17
2.5.3 Comparative studies 17
Box 2.1 The basic evolutionary forces 11
Box 2.2 The disease space 13
3 The diversity and natural history of parasites 19
3.1 The ubiquity of parasites 19
3.2 A systematic overview of parasites 21
3.2.1 Viruses 21
3.2.2 Prokaryotes 22
3.2.2.1 Archaea 23
3.2.2.2 Bacteria 23
3.2.3 The basal eukaryotes 24
3.2.4 Protozoa 25
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viii CONTENTS
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 31
3.2.10 Crustacea 31
3.2.11 Mites (Acari), ticks, lice (Mallophaga, Anoplura) 33
3.2.12 Parasitic insects (parasitoids) 34
3.3 The evolution of parasitism 34
3.3.1 Evolution of viruses 35
3.3.2 Evolution of parasitism in nematodes 36
3.4 The diversity and evolution of parasite life cycles 37
3.4.1 Steps in a parasite’s life cycle 37
3.4.2 Ways of transmission 39
3.4.3 Complex life cycles 40
3.4.4 The evolution of complex parasite life cycles 41
3.4.5 Example: trypanosomes 45
3.4.6 Example: helminths 46
Box 3.1 Types of parasites 20
4 The natural history of defences 51
4.1 The defence sequence 51
4.1.1 Pre- infection defences 52
4.1.1.1 Avoidance behaviour 52
4.1.1.2 The selfish herd and group-living 52
4.1.1.3 Anticipatory defences 52
4.1.1.4 ‘Genetic’ defences 54
4.1.2 Post- infection defences 54
4.1.2.1 Behavioural changes 54
4.1.2.2 Physiological responses 56
4.1.3 Social immunity 57
4.2 Basic elements of the immune defence 59
4.2.1 Humoral defences 60
4.2.1.1 Immunoglobulins 60
4.2.1.2 Complement 60
4.2.1.3 Other humoral components 61
4.2.2 Cellular defences 62
4.2.2.1 Haematopoiesis (cell development) 63
4.2.2.2 Phagocytosis 65
4.2.2.3 Melanization, encapsulation 67
4.2.2.4 Clotting, nodule formation 67
4.3 Basic defences by the immune system 68
4.3.1 Inflammation 68
4.3.2 Innate immunity 68
4.3.3 Adaptive (acquired) immunity 69
4.3.4 Regulation of the immune response 69
4.3.4.1 Regulation by protein–protein interactions 70
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CONTENTS ix
4.3.4.2 Regulation by miRNAs 70
4.3.4.3 Regulation by post- translational modification 70
4.3.4.4 Negative regulation 72
4.4 Immune defence protein families 72
4.4.1 The major families 74
4.4.2 Effectors: antimicrobial peptides 76
4.5 The generation of diversity in recognition 77
4.5.1 Polymorphism in the germline 78
4.5.2 Somatic generation of diversity 78
4.5.2.1 Alternative splicing 78
4.5.2.2 Somatic DNA modification 79
4.5.2.3 Somatic (hyper-)mutation, gene conversion 81
4.5.3 Variability and B- and T- cells 81
4.5.3.1 B- cells 81
4.5.3.2 T- cells 84
4.6 The diversity of immune defences 85
4.6.1 Defence in plants 85
4.6.2 Defence in invertebrates 89
4.6.2.1 Insects 89
4.6.2.2 Echinoderms 91
4.6.3 The jawed (higher) vertebrates 92
4.7 Memory in immune systems 96
4.7.1 Memory in the adaptive system 98
4.7.2 Memory in innate systems 98
4.8 Microbiota 100
4.8.1 Assembly, structure, and location of the microbiota 100
4.8.2 Mechanisms of defence by the microbiota 102
4.9 Evolution of the immune system 104
4.9.1 Recognition of non- self 104
4.9.2 The evolution of signal transduction and effectors 104
4.9.3 The evolution of adaptive immunity 105
Box 4.1 Disease space: defences 54
Box 4.2 Adaptive immunity in prokaryotes: the CRISPR–Cas system 86
Box 4.3 Antiviral defence of invertebrates 90
Box 4.4 Priming and memory 97
5 Ecological immunology 109
5.1 Variation in parasitism 109
5.1.1 Variation caused by external factors 109
5.1.2 Variation in immune responses 110
5.2 Ecological immunology: The costs of defence 115
5.2.1 General principles 115
5.2.2 Defence costs related to life history and behaviour 118
5.2.3 Cost of evolving an immune defence 118
5.2.3.1 Genetic costs associated with the evolution of immune defences 118
5.2.3.2 Physiological costs associated with the evolution (maintenance)
of immune defences 120
