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


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


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


Cellular immunity assays


Forced co-habitation assays


Adaptive significance of behavioral avoidance


Sensory basis of behavioral avoidance


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.


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


Figure 6. Behavioral avoidance in sensory mutant strains.

44 Discussion 44 Acknowledgements 50

Chapter 2 Appendix


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


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.


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


Effects of ethanol consumption before and after exposure to wasps


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.


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


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


Figure 4. Larval ethanol food preference.


Figure 5. Adult ethanol oviposition preference.

78 Discussion 79 Acknowledgements 86

Chapter 3 Appendix


Figure S1. Additional larval ethanol food preference experiment.


Figure S2. Additional adult ethanol oviposition preference experiments.


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


Host and parasite populations


Experimental evolution


Host mortality rate assays


Measuring host outcrossing rates


Competitive fitness assays

101 Results 102

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


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


Table 1. Outcrossing rate contrasts.


Figure 3. Host adaptation to parasites.


Figure 4. Mortality rates of evolved hosts when exposed to Sm2170.

107 Discussion 107 Acknowledgements 112

Chapter 5: Conclusion

113 References 119

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