Ecological immunology in a tri-trophic context: plant-mediated defense and immune gene evolution in monarch butterflies 公开
Tan, Wen-Hao (Spring 2019)
Published
Abstract
Animals have evolved multiple forms of defense against parasites. Animal defense is often studied in the context of pairwise interactions between hosts and parasites, but the environmental context in which they interact can also shape animal defense. For instance, toxic plant secondary chemicals can increase herbivore defense against their enemies. Thus, specialization on toxin-producing plants may shape the evolution of other herbivore defenses, leading to variation within and between populations. In this dissertation, I used monarch butterflies (Danaus plexippus) to examine plant-mediated defense and immune gene evolution in a tri-trophic context involving the butterflies, their parasites (Ophryocystis elektroscirrha), and their milkweed hostplants (Asclepias spp.). In this system, milkweed species affects monarch resistance to the parasites, and this difference in resistance is correlated with plant toxicity. First, I studied how milkweed inducible toxin production upon herbivory affects monarch parasite resistance. I found that interspecific variation in plant toxicity is a more important driver of parasite resistance than plasticity in toxin production via induction. Second, I studied changes in global gene expression of monarchs in response to milkweed diet and parasite infection, and the interplay between plant toxins and herbivore immunity. I found that monarchs differentially express several hundred genes when feeding on plant species that differ in toxicity, including genes belonging to multiple families of canonical detoxification genes, which may play a role in toxin resistance and sequestration. Also, I found that a small number of immune genes were down-regulated when feeding on a more toxic plant. Third, I studied the evolution of canonical immune genes across different monarch populations that vary in their association with milkweed species and parasite prevalence. I found that different classes of immune genes exhibit different patterns of selection, differentiation, and polymorphism. For example, signaling genes exhibit signals of purifying selection while effector genes show signatures of balancing selection. I also found some population-specific patterns, suggesting that monarch immune genes are not under uniform selection across geographically, genetically and ecologically distinct populations. By combining experimental approaches, studies of gene expression, and population genomic analyses, this study increases our understanding of the evolutionary ecology of herbivore immunity.
Table of Contents
Chapter 1: Introduction 1
1.1 Immunity in a tri-trophic context 1
1.2 Plant-mediated effects on herbivore defenses 1
1.3 Evolution of herbivore immunity in association with toxic phytochemicals 5
1.4 Monarch butterflies as a study system 7
Chapter 2: The effects of milkweed induced defense on parasite resistance in monarch butterflies, Danaus plexippus 14
Abstract 14
2.1 Introduction 15
2.2 Methods and Materials 16
2.3 Results 19
2.4 Discussion 22
2.5 Acknowledgments 23
Chapter 3: Transcriptomics of monarch butterflies reveals strong differential gene expression in response to host plant toxicity, but weak response to parasite infection 25
Abstract 25
3.1 Introduction 26
3.2 Materials and Methods 30
3.3 Results 37
3.4 Discussion 54
3.5 Conclusions 61
3.6 Acknowledgments 62
3.7 Supplemental Information 63
Chapter 4: Population genomics reveals complex patterns of immune gene evolution in monarch butterflies (Danaus plexippus) 68
Abstract 68
4.1 Introduction 69
4.2 Materials and Methods 73
4.3 Results 80
4.4 Discussion 108
4.5 Conclusions 116
4.6 Acknowledgments 117
4.7 Supplemental Information 118
Chapter 5: Conclusions and future directions 131
5.1 Discussion of Chapter 2 131
5.2 Discussion of Chapter 3 133
5.3 Discussion of Chapter 4 135
Bibliography 138
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Ecological immunology in a tri-trophic context: plant-mediated defense and immune gene evolution in monarch butterflies () | 2019-05-07 23:50:24 -0400 |
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