Ecological factors determine immune costs and susceptibility of pea aphids to a natural fungal pathogen Open Access

Parker, Benjamin James (2013)

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Studying the immune system in the context of ecology has been critical for our understanding of host-parasite interactions. Fundamental to this approach is the recognition that immunity is costly to organisms. From this research field we have learned that internal constraints caused by the high costs of immunity have frequently led to measurable variation among individuals in parasite defense. Understanding the factors influencing the evolution of host defenses is of interest not just because of the devastating effects of parasites on host populations, but also for understanding a major class of interspecific interactions.

However, studies frequently fail to measure immune costs. One explanation is that immune responses only impact host fitness under certain ecological conditions. Studies have implicated host nutrition as one such condition, but it is likely that other ecological factors play an important role as well. In this dissertation, I use pea aphids (Acrythosiphon pisum) and their natural microbial communities to study how ecological factors influence susceptibility to pathogens and the link between immunity and host fitness. I first measure aphid reproductive fitness in response to several natural microbial pathogens, and demonstrate that exposure to several aphid-specific fungal pathogens is costly. I then show that the expression of these costs is influenced by ecological factors: exposure to environmental stressors that lead to the production of a winged dispersing morph, and the presence of intracellular bacteria that protect their hosts from fungal pathogens. By combining experiments, immune assays, and measures of gene expression, this work aims to increase our understanding of the link between immunity and host fitness, and to enhance our mechanistic understanding of immune costs.

Table of Contents

Chapter 1: Introduction 1

Costs of immunity ... 1

Investment in Immunity and Context-Dependent Costs ... 4

The Invertebrate Immune System ... 6

Aphids and Their Microbial Community ... 10

Chapter 2: Exposure to natural pathogens reveals costly aphid response to fungi but not bacteria ... 16

Introduction ... 17

Methods ... 18

Results ... 22

Discussion ... 26

Supplementary Figures ... 29

Chapter 3: Increased pathogen susceptibility and immune costs in a dispersal polyphenism ... 32

Introduction ... 33

Results & Discussion ... 35

Conclusions ... 49

Methods ... 51

Supplementary Information ... 58

Chapter 4: Genetic variation in resistance and fecundity tolerance in a natural host-pathogen interaction ... 67

Introduction ... 68

Methods ... 71

Statistical Methods ... 74

Results ... 75

Discussion ... 81

Supporting Information ... 84

Chapter 5: Symbiont-mediated protection against fungal pathogens in pea aphids: a role for pathogen specificity? ... 87

Zoophthora (specialist) infection: ... 90

Beauveria (generalist) infection: ... 92

Supporting Information ... 96

Chapter 6: Immune Costs in the Presence of Protective Microbes ... 105

Introduction ... 105

Methods ... 107

Results ... 110

Discussion ... 113

Chapter 7: Conclusions ... 116

References ... 123

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