Effects of parasites on host adaptation: immune system trade-offs, alternative behavioral defenses, and outcrossing rates Open Access

Lynch, Zachary R. (2016)

Permanent URL: https://etd.library.emory.edu/concern/etds/xk81jm066?locale=en
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Abstract

Coevolution between hosts and parasites drives adaptation in both antagonists; hosts are selected to resist or tolerate infection and parasites are selected to optimize their infectivity and transmission. Host immune systems comprise behavioral, cellular, humoral, social, and symbiont-mediated defenses, which can alleviate the fitness consequences of infection but may carry maintenance and deployment costs. Therefore, hosts are expected to specialize in only a subset of possible defenses. I tested this hypothesis by measuring behavioral and cellular defenses used by fruit flies against parasitoid wasps. However, I found no evidence for trade-offs in the relative strengths of these defenses across eight fly species and two wasp species. Although one wasp species was more virulent, each fly species behaved similarly towards both wasps. Drosophila melanogaster exhibited the weakest cellular immunity and the strongest behavioral avoidance, suggesting that it may specialize in alternative defenses against wasps, such as medication with ethanol. I found that fly larvae experienced a two-fold reduction in parasitization intensity when they consumed ethanol during exposure to the generalist wasp Leptopilina heterotoma, leading to a 24-fold increase in survival to adulthood. However, larvae did not self-medicate with ethanol after being parasitized. Instead, my results suggest that female flies have an innate preference for laying eggs in ethanol food, a behavior that protects their offspring from wasps but occurs independent of wasp exposure. My final chapter addresses a central mystery in evolutionary biology: why is outcrossing ubiquitous in plants and animals despite its reduced population growth potential relative to self-fertilization? The best-supported explanation is that host-parasite coevolution generates shifting adaptive landscapes that favor outcrossed offspring. I tested whether parasite turnover could have a similar effect in the absence of coevolution. Using experimental evolution with the nematode Caenorhabditis elegans and the pathogenic bacterium Serratia marcescens, I found that exposure to novel parasite strains led to elevated host outcrossing rates, which facilitated host adaptation. My results suggest that recurring episodes of parasite turnover could favor the long-term maintenance of outcrossing. Future studies should investigate behavioral defenses using more ecologically realistic experimental setups and host-parasite combinations with more recent coevolutionary histories.

Table of Contents

Chapter 1: Introduction 1

History of trade-off research 2

Costs of humoral and cellular immune responses 5

Costs of behavioral immune responses 7

Immune trade-offs within species 9

Immune trade-offs across species 12

The role of outcrossing in host adaptation 14

Overview of dissertation research 17

Chapter 2: Evolution of behavioural and cellular defences against parasitoid wasps in the Drosophila melanogaster subgroup 20

Abstract 20

Introduction 21

Materials and Methods 26

Insect strains and maintenance 26

Cellular immunity assays 29

Forced co-habitation assays 30

Adaptive significance of behavioral avoidance 31

Sensory basis of behavioral avoidance 32

Phylogenetic analysis 32

Figure 1. Phylogeny of the eight fly species. 34

Statistical analysis 34

Results 37

Figure 2. Cellular immunity indices 38

Figure 3. Oviposition maintenance indices 39

Figure 4. Cellular immunity and oviposition maintenance correlations 40

Figure 5. Testing for an offspring quality vs. quantity trade-off in D. yakuba 42

Figure 6. Behavioral avoidance in sensory mutant strains 44

Discussion 44

Acknowledgements 50

Chapter 2 Appendix 52

Table S1. Cellular immunity dish replicates (reps), eclosion outcomes, and cellular immunity indices 52

Table S2. Forced co-habitation vial replicates (reps), cumulative per-female egg counts (PFEC), and oviposition maintenance indices (OMI) 52

Table S3. Sources for Amyrel coding sequences 53

Figure S1. Testing for an offspring quality vs. quantity trade-off in D. melanogaster and D. simulans 55

Chapter 3: Ethanol confers differential protection against generalist and specialist parasitoids of Drosophila melanogaster 57

Abstract 57 Introduction 58

Materials and Methods 62

Insect strains and maintenance 62 Recipes for colored ethanol solutions 63

Effects of ethanol consumption on unparasitized larvae 64

Effects of ethanol consumption before and after exposure to wasps 64

Effects of ethanol consumption during exposure to wasps 65

Larval ethanol food preference 66

Adult ethanol oviposition preference 67

Results 69

Figure 1. Effects of ethanol consumption on unparasitized larvae 70

Figure 2. Effects of ethanol consumption before and after exposure to wasps 71

Figure 3. Effects of ethanol consumption during exposure to wasps 74

Figure 4. Larval ethanol food preference 76

Figure 5. Adult ethanol oviposition preference 78

Discussion 79

Acknowledgements 86

Chapter 3 Appendix 87

Figure S1. Additional larval ethanol food preference experiment 88

Figure S2. Additional adult ethanol oviposition preference experiments 89

Chapter 4: Turnover in local parasite populations favors host outcrossing over self-fertilization during experimental evolution 90

Abstract 90

Introduction 91

Materials and Methods 96

Study system 96

Host and parasite populations 97

Experimental evolution 98

Host mortality rate assays 99

Measuring host outcrossing rates 100

Competitive fitness assays 101

Results 102

Figure 1. Mortality rates of ancestral hosts when exposed to the four parasite strains 103

Figure 2. Changes in host outcrossing rates during experimental evolution 105

Table 1. Outcrossing rate contrasts 105

Figure 3. Host adaptation to parasites 106

Figure 4. Mortality rates of evolved hosts when exposed to Sm2 170. 107

Discussion 107

Acknowledgements 112

Chapter 5: Conclusion 113

References 119

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