Determining the effects of animal migration and range expansion on population genetics Open Access

Pierce, Amanda (2015)

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Animal movement does not only affect the individual, but can also have profound implications for population dynamics and species distributions. In this thesis, I use the monarch butterfly, Danaus plexippus, as a model system to understand the connectivity and genetic differentiation among populations with different migratory strategies, as well as the effects of range expansion on population genetics and structure. Monarchs are known for their fall migration from eastern North America to their overwintering sites in Mexico, but also occur west of the Rocky Mountains, from which they migrate to the California coast. Using microsatellite markers, I found that despite differences in migration destination and the Rocky Mountains to serve as a potential barrier, eastern and western North American monarchs are genetically indistinguishable. This indicates that monarchs are able to maintain divergent migratory pathways despite high genetic similarity. I expanded this study to include additional sampling sites located south of the Mexican overwintering sites. It has long been believed that monarchs have a two-way migration in which all monarchs return north after the overwintering period. However, I found that monarchs in Costa Rica and Belize are not genetically differentiated from their northern counterparts. A hypothesis is that rather than a strict two-way migration, some percentage of monarchs instead radiate outwards from the overwintering sites. Moreover, the monarchs in Costa Rica and Belize are non-migratory, which again demonstrates how different migratory strategies are maintained despite high similarity among neutral genetic sites. In addition to the monarchs mentioned, there are also non-migratory monarchs located around the world wherever temperature and larval food plant abundance allow. Despite monarchs colonizing these locations fairly recently, my research found high levels of genetic structure and differentiation across areas and continents that are separated by seas and oceans. My work also suggests that despite the high proclivity for dispersal, genetic drift still plays a major role in shaping allele frequencies in these newly colonized areas, through multiple and serial founder effects. Future work coupling population genetic theory with next generation technologies will lead to additional breakthroughs in this field.

Table of Contents

Chapter 1: Introduction

1.1 Animal dispersal and its effects on population genetics 2

Figure 1.1 Genetic drift occurring at the wave front 4

1.2 Animal migration genetics and its effect on population structure 5

1.3 Using monarch butterflies as a model system 7

Figure 1.2 Overwintering sites of eastern and western monarchs 8

Figure 1.3 Map showing location and migration patterns 9

Figure 1.4 Worldwide distribution of monarchs 10

1.4 Summaries of Chapters 2, 3, 4, 5, and 6 12

Chapter 2: Lack of genetic differentiation between monarchs with divergent migration destinations

2.1 Introduction 15

Figure 2.1 Map showing location and migratory patterns of sampled populations 17

2.2 Materials and Methods 18

Table 2.1 Microsatellite loci developed in this study 19

Table 2.2 Observed and expected heterozygosity at each locus 21

2.3 Results 24

Figure 2.2 Inferred genetic proportion of butterflies to each population 25

Table 2.3 Pairwise FST and RST values 26

Figure 2.3 Isolation by distance 27

Figure 2.4 Measures of genetic diversity 28

Table 2.4 Results of Analysis of Molecular Variance 29

Figure 2.5 Statistical power to detect significant population differentiation 29

2.4 Discussion 30

Chapter 3: Unraveling the mysteries of monarch migration and global dispersal through molecular genetic techniques

3.1 Introduction 34

3.2 Allozyme markers show seasonal mixing and shed light on origins of Pacific monarchs 35

Figure 3.1 Worldwide distribution of monarchs 38

3.3 East meets west: on the origins of and mixing between North American monarchs 38

Figure 3.2 East meets west 40

3.4 Does open water impede gene flow? 43

Figure 3.3 Location and hypothesized dispersal of sampled monarch populations 44

Figure 3.4 Inferred genetic proportion of individual butterflies to 7 populations 45

Table 3.1 Pairwise FST and RST values 47

3.5 A new view of monarch migration and evolution in the genomic era 48

3.6 Outlook 50

Chapter 4: Serial founder effects and genetic differentiation during worldwide range expansion of monarch butterflies

4.1 Introduction 52

Figure 4.1 Map showing sampling locations 54

4.2 Methods 55

Table 4.1 Sampling sites and numbers of monarch butterflies 55

4.3 Results 58

Figure 4.2 Worldwide structure plot 59

Figure 4.3 Distance tree based on Nei's standard genetic distance 60

Figure 4.4 Genetic trends across the Pacific 62

Figure 4.5 Genetic trends across the Atlantic 64

4.4 Discussion 64

4.5 Supplementary Figures/Tables

Table S4.1 Observed and expected heterozygosity 69

Table S4.2 Pairwise FST and RST values 71

Table S4.3 Pairwise FST and RST values based on corrected alleles 73

Figure S4.1 Principal Coordinate Analysis 75

Figure S4.2 Allelic clinal pattern across Pacific 76

Figure S4.3 Allele frequencies across the Atlantic 77

Chapter 5: Extreme heterozygosity in parasitism despite low population genetic structure among monarch butterflies inhabiting the Hawaiian Islands

5.1 Introduction 78

Figure 5.1 Variation in parasite prevalence on four islands of Hawaii 81

5.2 Materials and Methods 81

Table 5.1 Monarchs sampled in Hawaii by collection site and year 82

5.3 Results 87

Figure 5.2 Proportion of monarchs heavily infected with OE 88

Table 5.2 Results of the analysis of molecular variance 89

Table 5.3 Pairwise FST and RST values 90

Figure 5.3 Structure plot showing K=2 91

Figure 5.4 Measures of genetic diversity 93

5.4 Discussion 93

5.5 Supplementary Materials 96

Table S5.1 Field collection site variables 96

Table S5.2 Monarchs used for genetic analysis 97

Table S5.3 Microsatellite loci used in this study 98

Table S5.4 Observed and expected heterozygosity 99

Table S5.5 Pairwise FST and RST values 100

Figure S5.1 Structure plot showing that K=1 100

Chapter 6: Summary and Conclusions

6.1 Animal dispersal and its effects on population genetics 101

6.2 Animal migration and its effects on population genetics 103

6.3 Future directions: from population genetics to population genomics 105

Bibliography 109

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