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Overview

"This excellent book offers much food for thought. The scholarship is as sound as any one human can make it, and the smooth writing carries one along nicely. Evolutionary Ecology of Parasites will not only be a valuable resource in graduate seminars, it will also help researchers get a handle on the literature and the major questions in the field."—Janice Moore, Colorado State University, author of Parasites and the Behavior of Animals

"This is an important book. I am glad there is someone out there with the brains and guts to tackle the diverse body of literature summarized here."—Dale H. Clayton, University of Utah

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Editorial Reviews

Journal of Parasitology - Gerald Esch
What a wonderful book! . . . I can heartily recommend this volume for all parasitologists, regardless of their specific research interests, and whether students or teachers. I would also strongly recommend this book for the 'non-parasite' ecologist and evolutionary biologist because it will provide them with a concise picture of how parasites fit into the general scheme of ecology and evolution, something about which they really should know a lot, but many times do not! Poulin does, and explains it well.
From the Publisher
"What a wonderful book! . . . I can heartily recommend this volume for all parasitologists, regardless of their specific research interests, and whether students or teachers. I would also strongly recommend this book for the 'non-parasite' ecologist and evolutionary biologist because it will provide them with a concise picture of how parasites fit into the general scheme of ecology and evolution, something about which they really should know a lot, but many times do not! Poulin does, and explains it well."—Gerald Esch, Journal of Parasitology

Journal of Parasitology
What a wonderful book! . . . I can heartily recommend this volume for all parasitologists, regardless of their specific research interests, and whether students or teachers. I would also strongly recommend this book for the 'non-parasite' ecologist and evolutionary biologist because it will provide them with a concise picture of how parasites fit into the general scheme of ecology and evolution, something about which they really should know a lot, but many times do not! Poulin does, and explains it well.
— Gerald Esch
Journal of Parasitology
What a wonderful book! . . . I can heartily recommend this volume for all parasitologists, regardless of their specific research interests, and whether students or teachers. I would also strongly recommend this book for the 'non-parasite' ecologist and evolutionary biologist because it will provide them with a concise picture of how parasites fit into the general scheme of ecology and evolution, something about which they really should know a lot, but many times do not! Poulin does, and explains it well.
— Gerald Esch
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Product Details

  • ISBN-13: 9780691120843
  • Publisher: Princeton University Press
  • Publication date: 12/11/2006
  • Edition description: 2ND
  • Edition number: 2
  • Pages: 342
  • Product dimensions: 7.20 (w) x 10.00 (h) x 1.00 (d)

Meet the Author

Robert Poulin is Professor of Zoology at the University of Otago, New Zealand. He is the coauthor of "Parasite Biodiversity" and the editor of two other books.

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Read an Excerpt

Evolutionary Ecology of Parasites


By Robert Poulin

Princeton University Press

Copyright © 2006 Princeton University Press
All right reserved.




Chapter One

INTRODUCTION

Ecology is the scientific study of interactions between organisms of the same or different species, and between organisms and their nonliving environment. One of the main goals of ecologists is to explain the abundance and distribution of organisms over space and time. The scope of ecology includes all sorts of interactions, from the most intimate, permanent associations to the briefest of encounters. Although parasitism qualifies as the sort of interaction of interest to ecologists, it has somehow become the focus for another branch of science, parasitology, which uses a multidisciplinary approach to investigate host-parasite interactions. Because of the intimate and intricate nature of the association between host and parasite, a broadly trained parasitologist using techniques ranging from molecular biology all the way to ecology seemed the most appropriate investigator. The problem with this takeover of parasitism by parasitologists, however, is that parasites have been ignored by ecologists for a long time. Sections on parasitism have only recently begun to appear in ecology textbooks (for instance, Begon et al. 2005 and earlier editions), and these bear mainly on the ecological impacts of parasites on free-living organisms. Studies on the population or community ecology of parasites themselves are practically absent from theecology literature; they are almost exclusively restricted to parasitology journals, and often devoid of any references to important ecological studies on free-living animals.

Similarly, parasite evolution has until recently been studied by parasitologists rather than by evolutionary biologists. As with ecological studies, evolutionary investigations of host-parasite interactions undertaken by nonparasitologists are relatively recent (Poulin 1995a), but rapidly growing in number. While the quality of studies on the ecology or evolution of parasitism performed by parasitologists is not in doubt, it is unfortunate that for many years there have been few exchanges of ideas between parasitology and either ecology or evolutionary biology. Researchers in these disciplines attend different meetings and read different journals. Ecologists and parasitologists have even developed their own jargon; although they use similar terms, they assign different meanings to the same words, which hinders effective communication between the two disciplines (Bush et al. 1997). More importantly, the separation between parasitology, ecology, and evolutionary biology has lead to philosophical differences between these branches of biology, some of which are important. For instance, parasitologists have long known that parasites can affect host population dynamics, but ecologists took some time to realize this. Similarly, ecological parasitology developed as a discipline, in the mid- to late twentieth century, with strong doses of natural history and field biology; this period is beautifully captured, with a hint of nostalgia, by Esch's (2004) historical essays. During that time, however, most theoretical advances in ecology and evolutionary biology were ignored by parasitologists; those that were eventually adopted by parasitologists were only applied to parasites years after their introduction in other fields. For example, until recently and in part because of the influence of medical science on parasitology, many parasitologists accepted that evolution led to a decrease in parasite virulence, whereas modern evolutionary theory would have predicted a greater range of outcomes (Anderson and May 1982, 1991; Ewald 1994). These disagreements could have been avoided had there been a better integration of ecology, evolution, and knowledge of parasite biology by students of parasitism.

My purpose in this book is generally the same as in the first edition: to present an evolutionary ecologist's view of the biology of parasites. I want to discuss various aspects of the biology of parasites using an approach compatible with current theory in evolutionary biology and ecology. Many studies of parasite ecology or evolution published in the past fifty years were thorough descriptive investigations but failed to test the general hypotheses put forward by ecologists and evolutionary biologists; here I will try to rectify this by emphasizing the link with theory. In this book I approach parasites as an evolutionary ecologist would approach any other group of organisms, while recognizing the special attributes of parasites. The book focuses on parasites themselves rather than on the interaction with hosts. Instead, hosts are seen as a key part of the parasite's environment and as a major source of selective pressures. The influence of parasites on host biology has been dealt with extensively in recent reviews; it will only be covered here if it relates to the ecology or evolution of parasites.

My other objective is to suggest a research agenda for the next several years. Where relevant, I point out the gaps in our knowledge, and try to suggest ways of filling these gaps. With this book, I want to capture the present state of parasite ecology and evolution, and propose directions for its future growth.

1.1 The Evolutionary Ecology Approach

Organisms interact with one another and with the nonliving environment on an ecological time scale, measured in days, months, or years. These interactions, however, are the product of natural selection acting over evolutionary time, over thousands and millions of years, to produce organisms well suited to their environment. Evolutionary ecology is the study of the selective pressures imposed by the environment, and the evolutionary responses to these pressures. Natural selection has shaped not only the traits of individual organisms, but also the properties of populations and species assemblages. The subject matter of evolutionary ecology, therefore, includes topics such as the trade-off between the size and number of offspring produced by individual animals, the proportion of males and females in animal populations, and the composition of animal communities. All these phenomena can be studied on a human time scale but to understand the differences observed among organisms, one must consider the forces and constraints that have acted during their evolutionary history.

The study of evolutionary responses is not always as straightforward as that of phenomena occurring on shorter time scales. A major goal of science is to demonstrate causality; it can be inferred that an event causes a response if the response always follows the event in an experimental situation. For example, exsheathment of many nematode larvae and hatching of many cestode eggs always follow their exposure to the conditions encountered in their host's gut in in vitro experiments, therefore it can safely be inferred that these conditions cause exsheathment or hatching, at least in a proximate sense. In evolutionary ecology, the manipulation of variables in controlled experiments is often impossible. Instead, we must rely heavily on comparisons between species that have been exposed to different selective pressures. If species under a given selective regime have consistently evolved a certain combination of traits, these "natural" experiments can be used to draw conclusions about the effects of certain factors over evolutionary time. Obviously, similarity between species can be the result of inheritance of traits from a common ancestor as much as the product of independent lines of convergent evolution. A careful distinction must be made between phylogenetic influences and the true action of natural selection (Brooks and McLennan 1991; Harvey and Pagel 1991). In the absence of other evidence, comparisons across taxa can help to identify true adaptations, defined here as genetically determined traits that have spread or are spreading through a population because they confer greater fitness on their bearers.

Although only applied recently to parasitological problems, the comparative approach can shed much light on parasite evolution. This approach can do more than identify relationships between species traits. It can also be used to test evolutionary hypotheses even though it does not follow the classical experimental approach consisting of the manipulation of independent variables in controlled conditions (see Brandon 1994). Different parasite lineages leading to extant species can be viewed as different evolutionary experiments, in which the ancestor represents the initial experimental conditions and the current phenotype represents the experimental outcome. Comparing lineages evolving under different selective pressures (e.g., in different types of hosts) is like comparing the responses of subjects exposed to different experimental conditions, or their responses to the manipulation of selected variables. In this context, controlling for phylogenetic influences corresponds to avoiding pseudoreplication.

Proper comparative analyses are powerful tools for hypothesis testing in evolutionary ecology (Harvey and Pagel 1991). They are not, however, a panacea for the study of adaptation. Used in isolation from other kinds of evidence, comparative studies provide limited insights into evolutionary mechanisms and the causal links between biological traits (Doughty 1996). On the other hand, the comparative approach is the most useful to identify general patterns that can guide further research. Although the results of controlled experiments or field observations are used as tests of theory wherever possible throughout the book, much of the evidence presented in this book relies on the explanation of variability among species using a comparative approach.

At the same time as the comparative approach became a major tool for evolutionary biologists, a parallel development provided ecologists with a new way of tackling the complexity of natural systems. Macroecology has emerged as a research program aimed at trying to infer the laws of nature from the statistical patterns among its constituent parts (Brown 1995; Gaston and Blackburn 2000). Macroecology consists of the empirical detection of patterns, the formulation of mechanistic hypotheses to account for these patterns, and the empirical testing of the hypotheses. As a whole, macroecology has been remarkably successful at finding general patterns and likely explanations for these patterns (Brown 1995, 1999; Lawton 1999; Gaston and Blackburn 2000; Blackburn and Gaston 2001). Much of the information on parasite ecology presented in this book borrows strongly from the macroecological approach.

The comparative approach in both evolutionary biology and macroecology focuses on large-scale, general phenomena rather than on detail. As a rule, they provide broad, though sometimes tentative, answers to important questions instead of definitive answers to very specific questions. An effort is made throughout this book to combine evidence from comparative or macroecological studies with that from experimental studies, to provide different perspectives on the same problems.

This book is not an elementary treatise of evolutionary ecology. The reader who wants a more general overview of the theory and mathematical models at the core of modern evolutionary ecology can read any of several recent texts on the subject (e.g., Cockburn 1991; Bulmer 1994; Pianka 1994; Fox et al. 2001). This book applies many ideas from evolutionary ecology specifically to parasites, and aims to foster the use of evolutionary thinking in the study of parasite ecology. Some of the questions that will be addressed include: Why do some parasites have more complex life cycles than others? Why are some parasites more host-specific than others? Why are some parasites much more fecund than others? Why are some parasites much more virulent than others? Why are some parasites more highly aggregated among their hosts than others? Why is there greater gene flow among populations in some parasite species than in others? Why are some parasite communities richer than others? These questions have been addressed before by parasitologists, but usually not in an evolutionary context or not with appropriate comparative methods.

1.2 Scope and Overview

Because of its vague definition, the term parasite has been applied to a wide range of plant and animal taxa. One can even argue that parasites sensu lato greatly outnumber free-living organisms (Windsor 1998). The most widely accepted definition of a parasite is that it is an organism living in or on another organism, the host-feeding on it, showing some degree of structural adaptation to it, and causing it some harm (when the harm incurred by the host invariably leads to its death, the parasite is often referred to as a parasitoid). Interpretations of this definition vary among authors (see Zelmer 1998). Price (1980) included phytophagous insects as parasites, but excluded blood-sucking flies. Barnard (1990) included behavioral parasites, such as many birds that are not physiologically dependent on their host but exploit it in other ways, for example by stealing food from the host. Combes (1995, 2001) even included strands of DNA among parasitic entities. To avoid confusion, it is therefore necessary to specify the taxonomic scope of this book, which will focus exclusively on protozoan and metazoan parasites of animals. These include several diverse taxa of parasites (table 1.1) that have had several independent evolutionary origins. Because helminths and arthropods have been the subject of the majority of relevant studies, they will provide most examples. The general biology and life cycles of these parasites are described in detail in any basic parasitology text (e.g., Noble et al. 1989; Schmidt and Roberts 1989; Cox 1993; Roberts and Janovy 1996; Kearn 1998; Bush et al. 2001), and it will be assumed that the reader is at least superficially familiar with them. Some of the patterns discussed here and some of the conclusions they suggest may also apply to other groups of parasites, but these are beyond the scope of this book.

The evolutionary ecology of parasites can be studied at several hierarchical levels. The smallest unit of study in ecology is the individual organism, but ecologists also deal with populations of individuals of the same species, and with communities made up of several populations of different species. This book first examines how ecological traits of individual parasites have evolved, and then considers population and community characteristics. Chapter 2 begins with a discussion of how organisms that made a transition to parasitism from a free-living ancestral lifestyle have undergone changes in their biology; it also considers how historical events and selective pressures have shaped complex life cycles, and how these life cycles in turn have influenced the ecology of the parasites adopting them. Chapter 3 explores the reasons why some parasites have evolved the ability to exploit a wide range of hosts whereas others are restricted to a single host species. For organisms often thought to be small, degenerate egg-production machines, parasites also show a tremendous range of life-history traits. Chapter 4 discusses how much of this variation is explained by selective pressures from the host or the physical environment, and how much is due to phylogenetic constraints. The final characteristic of individual parasites that will be considered is their ability to harm or manipulate the host. Far from evolving to become benign commensals, parasites can be selected to become highly virulent exploiters of host resources, or they can evolve the ability to control the physiology and behavior of their host for their own benefit. Chapter 5 explores the conditions under which host exploitation strategies can evolve toward these extremes.

One of the most easily described properties of animal populations is their distribution in space. Parasite populations are typically aggregated among their host individuals, but the degree of aggregation varies greatly over time and among populations and species of parasites. The opening chapter on parasite population ecology will examine the causes of aggregation, and some of its potential evolutionary consequences (chapter 6).

(Continues...)



Excerpted from Evolutionary Ecology of Parasites by Robert Poulin Copyright © 2006 by Princeton University Press. Excerpted by permission.
All rights reserved. No part of this excerpt may be reproduced or reprinted without permission in writing from the publisher.
Excerpts are provided by Dial-A-Book Inc. solely for the personal use of visitors to this web site.
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Table of Contents

Preface ix

Chapter 1 Introduction 1

1.1 The Evolutionary Ecology Approach 2
1.2 Scope and Overview 4

Chapter 2 Origins of Parasitism and Complex Life Cycles 8

2.1 Transitions to Parasitism 8
2.2 Specialization of Parasites 11
2.3 Complex Life Cycles: Historical Contingency or Adaptation? 14
2.3.1 Increases in Life-Cycle Complexity 14
2.3.2 Abbreviation of Complex Life Cycles 21
2.4 Evolutionary Consequences of Complex Life Cycles 25
2.4.1 Transmission and Infection 26
2.4.2 Sexual Reproduction 35
2.5 Conclusion 40

Chapter 3 Host Specificity 41

3.1 Measuring Host Specificity 41
3.2 Host-Parasite Coevolution and Host Specificity 48
3.2.1 Macroevolutionary Patterns 48
3.2.2 Microevolutionary Processes 54
3.3 Determinants of Host Specificity 60
3.4 Observed Patterns of Host Specificity 63
3.5 Conclusion 69

Chapter 4 Evolution of Parasite Life-History Strategies 70

4.1 Phenotypic Plasticity and Adaptation 71
4.2 Parasite Body Size 73
4.2.1 Changes in Size as Adaptations to Parasitism 73
4.2.2 Correlates of Body Size 79
4.2.3 Sexual Size Dimorphism in Parasites 85
4.3 Parasite Age at Maturity 87
4.4 Egg Production in Parasites 88
4.4.1 Correlates of Fecundity 89
4.4.2 Trade-offs and Strategies of Egg Production 90
4.5 Conclusion 95

Chapter 5 Strategies of Host Exploitation 96

5.1 The Evolution of Virulence 97
5.1.1 The Theory 98
5.1.2 Empirical Tests 102
5.2 Parasitic Castration and Host Gigantism 110
5.3 Manipulation of Host Behavior by Parasites 114
5.3.1 Adaptive Manipulation? 115
5.3.2 Evolution of Host Manipulation 121
5.3.3 Host Manipulation in a Multispecies Context 126
5.4 Manipulation of Host Sex Ratio by Parasites 130
5.5 Conclusion 132

Chapter 6 Parasite Aggregation: Causes and Consequences 134

6.1 Measuring Parasite Aggregation 135
6.1.1 Indices of Aggregation 135
6.1.2 Problems with the Measurement of Aggregation 139
6.2 Natural Patterns of Aggregation 141
6.3 Causes of Aggregation 144
6.4 Consequences of Aggregation 150
6.4.1 Effective Population Size and Genetic Diversity 151
6.4.2 Sex Ratio 154
6.4.3 Macroevolutionary Phenomena 158
6.5 Conclusion 159

Chapter 7 Parasite Population Dynamics and Genetics 160

7.1 Models of Parasite Population Dynamics 161
7.2 Density-Dependent Regulation 166
7.3 Selected Examples of Population Studies 172
7.3.1 The Cestode Bothriocephalus acheilognathi 172
7.3.2 The Nematode Cystidicola cristivomeri 173
7.3.3 The Nematode Cystidicoloides tenuissima 174
7.3.4 The Acanthocephalan Acanthocephalus tumescens 175
7.4 Patterns of Parasite Abundance 177
7.5 Genetic Structure of Parasite Populations 179
7.6 Conclusion 186

Chapter 8 Interactions between Species and the Parasite Niche 188

8.1 Numerical Responses to Competition 189
8.2 The Parasite Niche 194
8.3 Functional Responses to Competition 195
8.4 Evolutionary Niche Restriction 203
8.5 Conclusion 207

Chapter 9 Parasite Infracommunity Structure 209

9.1 Species Richness of Infracommunities 210
9.2 Nestedness in Infracommunities 215
9.3 Species Associations among Infracommunities 220
9.4 Species Recruitment and Infracommunity Structure 224
9.5 Species Abundance and Biomass in Infracommunities 227
9.6 Conclusion 231

Chapter 10 Component Communities and Parasite Faunas 233

10.1 Richness and Composition of Component Communities 234
10.2 Evolution of Parasite Faunas 241
10.3 Species Richness of Parasite Faunas 245
10.4 Biogeography of Parasite Diversity 253
10.5 Host Specificity and the Composition of Parasite Faunas 257
10.6 Conclusion 260

Chapter 11 Conclusion 262

11.1 Environmental Changes and Parasite Evolutionary Ecology 263
11.2 Parasite Control and Parasite Evolutionary Ecology 265
11.3 Future Directions 267

References 271
Index 325

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