Effects of parasites on host adaptation: immune system trade-offs, alternative behavioral defenses, and outcrossing rates Open Access
Lynch, Zachary R. (2016)
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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