The Role of Medicinal Food Plants Mediating the Gut Microbiome and Disease Resistance in Monarch Butterflies Restricted; Files Only

Abstract

Animals live in close association with microbes that are largely impacted by host diet and can play a role in modulating host resistance to parasites. Growing evidence across the animal kingdom demonstrates three separate relationships: (i) host diet modulates resistance to parasites; (ii) host diet alters the gut microbiome; and (iii) the gut microbiome modulates resistance to parasites. However, evidence for an indirect link between diet and parasite resistance, through modulation of the microbiome, remains lacking. My dissertation explores the role of environmental factors in the ecological context of host-parasite interactions. I use monarch butterflies (Danaus plexippus), their larval food plants (Asclepiasspp.), and a common natural protozoan parasite,Ophryocystis elektroscirrha as a model system to investigate these questions by performing fecal transplants based on alternative plant diets. Before experimentation, I outline the known links between each pairwise interaction. From these two-way interactions, I discuss the potential for the three-way interaction between the diet, microbiome and disease providing the framework for my dissertation. To determine the natural variation of monarch butterfly, I characterizegut microbial communities using 16S sequencing technology and quantify bacterial load using quantitative PCR across the monarch lifecycle when larvae are fed on one of two milkweed species. I find that monarch butterfly gut microbial community composition is relatively consistent throughout development, with the exception of adults. Milkweed diet influences the microbial diversity in early larval instars, but not in later larval instars. To determine if milkweed diet modulates the monarch gut microbiome to an anti-parasitic state, I use a set of fecal transplant experiments and measure disease outcome. I find that lower parasite loads were associated with high microbiome diversity and high microbial abundance. For microbial transplants, lower parasite loads were specifically associated with low relative abundances of Pantoea and unclassified Enterobacteriaceae and high relative abundances of Chryseobacterium, Pedobacterand unclassified Rhizobiales.My dissertation demonstrates that diet-mediated microbiome transplants can increase resistance to parasites and that Lepidopteran gut microbiomes can be a crucial functional driver of host fitness.

Table of Contents

Table of Contents

 

 

Chapter 1: Introduction………………………………….……………………………..1

            1.1 The Influence of Diet and Microbes on Host Defense…………………………....2

            1.2 Monarch Butterflies as a Study System……………………......………………….4

            1.3 Overview of Dissertation……………………......………………………...……....7

Chapter 2:Diet-microbiome-disease: Investigating diet’s influence on infectious disease resistance through alteration of the gut microbiome….....8

Abstract……………………………………………………………………………......8

            2.1 Introduction……………………......………………………………………….…...9

            2.2Diets modulate resistance to parasites……………………......………………….14

2.3 Diets alter gut microbiomes……………………………………………………...16       

            2.4Gut microbiomes modulate parasitism…………………………………………..22

            2.5 Experimental Approaches to Study Diet-Microbiome-Disease Interactions….....27

2.6 Conclusion……………………………………………………………………….29

2.7 Acknowledgments……………………………………………………………….30

Chapter 3: Alternative diets affect the monarch butterfly microbiome in early development………………………………….……………..………………….....32

            Abstract………………………………………………………………………….......32

            3.1 Introduction………………………...……………………......…………………..33

            3.2 Methods…………..……………………......………………………...…….........37

3.3 Results…………..……………………......………………………...……...........41

3.4 Discussion…………..……………………......………………………....……....54

3.5 Acknowledgements….……………………......………………………...……....57

Chapter 4: Diet indirectly alters parasite resistance through the gut microbiome in monarch butterflies………………………………………………..58

Abstract…………………………………………………………………………......58

            4.1 Introduction………………………...……………………......………………….59

            4.2 Methods…………..……………………......………………………...…….........63

            4.3 Results…………..……………………......………………………...……...........73

4.4 Discussion…………..……………………......………………………...…….....86

4.5 Acknowledgements…………..……………………......………………...……...91

Chapter 5: Conclusions and Future Directions………………………………...92

5.1 Discussion of Chapter 3…………………………….………………………......92

            5.2 Discussion of Chapter 4……………..…………………......…………………...93

            5.3 Potential Mechanisms of Resistance..…………………......…………………....94

5.4 Broader Impacts…………………....…………………......…………………….96

References………………………………………………………………….……………99

List of Figures

Figure 1.1 ……………………………………………..………….……………………….........5

Figure 2.1 …………………………….……………..…………………......……………….....12

Figure 2.2 …………………………………………..…………………......…………………..13

Figure 2.3 …………………………….……………..…………………......………………….26

Figure 3.1.…………………………………………..…………………......…………………..38

Figure 3.2 …………………………….……………..…………………......……………….....43

Figure 3.3 …………………………………………..…………………......…………………..44

Figure 3.4 …………………………….……………..…………………......……………….....45

Figure 3.5 …………………………….……………..…………………......……………….....50

Figure 3.6 …………………………………………..…………………......…………………..53

Figure 4.1 …………………………….……………..…………………......……………….....75

Figure 4.2 …………………………………………..…………………......…………………..77

Figure 4.3 …………………………….……………..…………………......………………….80

Figure 4.4 …………………………….……………..…………………......………………......81

Figure 4.5 …………………………………………..…………………......…………………..85

Figure S3.1.…………………………………………..…………………......…………………47

Figure S3.2.…………………………………………..…………………......…………………49

Figure S3.3.…………………………………………..…………………......…………………51

Figure S4.1.…………………………………………..…………………......…………………65    

Figure S4.2.…………………………………………..…………………......…………………67

Figure S4.3.…………………………………………..…………………......…………………68

Figure S4.4.…………………………………………..…………………......…………………79    

List of Boxes and Tables

Box 2.1………………………………..…………………………….……………………….....21

Box 2.2………………………………..…………………………….……………………….....31

Table 3.1………………………………..…………………………….………………………...46

Table 3.2………………………………..…………………………….………………………...46

Table 3.3………………………………..…………………………….………………………...46

About this Dissertation

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School	Laney Graduate School
Department	Biological and Biomedical Sciences
Degree	Ph.D.
Submission	Dissertation
Language	English
Research Field	Biology, Entomology Biology, Ecology Biology, Microbiology
关键词	host-parasite interactions host plants microbiome milkweeds ontogenetic development Ophryocystis elektroscirrha monarch butterflies
Committee Chair / Thesis Advisor	Jacobus C. de Roode, Ph.D., Emory University Nicole M. Gerardo, Ph.D., Emory University
Committee Members	Timothy D. Read, Ph.D., Emory University Joanna B. Goldberg, Ph.D., Emory University Gregory A. Dasch, Ph.D., Emory University

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