Population Genetics of Raccoons in the Eastern United States With Implications for Rabies Transmission and Spread Open Access

Abstract

Population Genetics of Raccoons in the Eastern United States
With Implications for Rabies Transmission and Spread

By
Serena Ann Reeder Carroll

A central research question in disease ecology concerns how a pathogen moves
throughout space and time (Anderson and May 1978). For directly transmitted zoonoses,
this process is likely influenced by the biological and environmental characteristics of
both the pathogen and its host (Real and McElhany 1996; Hess et al. 2001; Real and Biek
2007). Although these interactions are complex, one can attempt to discern the relative
contribution of each component by testing explicit hypotheses systematically. The
motivation for this research was to increase our understanding of how a directly
transmitted pathogen spreads in a wildlife population, and specifically, to examine host
factors that might influence pathogen transmission or spread.

In this dissertation, the raccoon rabies model system was used to explore how
social structure and landscape heterogeneity influence pathogen transmission. We used
genetic data to generate relatedness estimates of raccoons and tested whether social
organization influenced host contact rates or raccoon rabies transmission (Chapter 2).
Additionally, we used genetic data to define the historical and contemporary population
structure of raccoons throughout the range of the raccoon rabies virus variant (RRV).
This information was used to determine whether landscape heterogeneity in the form of
historically defined suture-zones (Remington 1968) in the eastern US resulted in limited
raccoon dispersal or barriers to gene flow that might also have affected the spread of
RRV (Chapter 3). Finally, surveillance data and modeling techniques were used to
examine the influence of host biology (home range, incubation, and infectious periods)
on the spatial and temporal clustering or aggregation of raccoon rabies in a multi-host
system, raccoons and skunks, in the northeastern US (Chapter 4). Each of the chapters
discusses the specific hypotheses tested and results in depth, and a summary can be found in Chapter 5.

Table of Contents

Chapter 1. Introduction 1

1.1 Background 1

1.2 Goals of the Dissertation 4

1.3 Raccoons and Rabies as a Model System 4

1.4 Population Genetics of Raccoons (Procyon lotor) Corresponding

to a New Focus of Raccoon Rabies in Northeastern Ohio:

Implications for Transmission 12

1.5 Historical and Contemporary Evolution Account for Population

Subdivision in Raccoon (Procyon lotor) Populations in the

Eastern United States 13

1.6 Spatiotemporal Interactions Of Enzootic Raccoon Rabies 14

Chapter 2. Population Genetics of Raccoons (Procyon lotor) Corresponding

to a New Focus of Raccoon Rabies in Northeastern Ohio:

Implications for Transmission 16

2.1 Introduction 16

2.2 Materials and Methods 21

2.2.1 Raccoon Samples and Collection Localities 21

2.2.2 DNA Isolation and Microsatellites 23

2.2.3 Mitochondrial DNA 25

2.2.4 Population Genetic Structure 26

2.2.5 Sex Ratio and Haplotype Distribution 27

2.2.6 Relatedness 28

2.3 Results 28

2.3.1 Microsatellites 28

2.3.2 Population Genetic Structure 29

2.3.3 Mitochondrial DNA 33

2.3.4 Rabid Versus Non-Rabid Raccoons 36

2.3.5 Relatedness 36

2.4 Discussion 39

Chapter 3. Historical and Contemporary Evolution Account for Population

Subdivision in Raccoon (Procyon lotor) Populations in the

Eastern United States 44

3.1 Introduction 44

3.1.1 Landscape Genetics and Relevance to Raccoon Rabies 44

3.1.2 Suture-Zones As Historic or Contemporary Barriers to

Gene Flow? 46

3.1.3 A Common Phylogeographic Boundary for the

Southeastern United States Eco-Region? 51

3.2 Materials and Methods 53

3.2.1 Raccoon Samples 53

3.2.2 DNA Isolation and Microsatellites 55

3.2.3 Population Genetic Structure 56

3.2.4 Mitochondrial DNA 57

3.2.5 Tests of Selective Neutrality 58

3.3 Results 59

3.3.1 Microsatellites 59

3.3.2 Population Genetic Structure 60

3.3.3 Mitochondrial DNA 63

3.3.4 Tests of Selective Neutrality 65

3.4 Discussion 66

3.4.1 Contemporary Population Structure and Barriers

to Gene Flow 66

3.4.2 Historical Population Structure and Barriers

to Gene Flow 68

3.4.3 Implications for a Southeastern US Eco-Region 69

3.4.4 Factors Influencing Raccoon Rabies Spread During

the 1950s-1970s 70

Chapter 4. Spatiotemporal Interactions of Enzootic Raccoon Rabies 73

4.1 Introduction 73

4.2 Materials and Methods 77

4.3 Results 82

4.4 Discussion 85

Chapter 5. Summary and Conclusions 89

References/Bibliography 93

About this Dissertation

Rights statement

• Permission granted by the author to include this thesis or dissertation in this repository. All rights reserved by the author. Please contact the author for information regarding the reproduction and use of this thesis or dissertation.

School	Laney Graduate School
Department	Biological and Biomedical Sciences
Subfield / Discipline	Population Biology, Ecology & Evolution
Degree	PhD
Submission	Dissertation
Language	English
Research Field	Biology, Genetics Biology, Ecology Biology, General
Keyword	phylogeography population genetics raccoons rabies
Committee Chair / Thesis Advisor	Real, Leslie, Emory University
Committee Members	Mills, James, CDC Thomas, James, Emory University Zwick, Michael, Emory University Rupprecht, Charles, CDC

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