University of Cincinnati

University of Cincinnati Date: 12/6/2010 I, Heather Farrington , hereby submit this original work as part of the requirements for the degree of Doctor of Philosophy in Biological Sciences. It is entitled: Historical Specimens Reveal a Century of Genetic Change in Darwin's Finches Student's name: Heather Farrington This work and its defense approved by: Committee chair: Kenneth Petren, PhD Committee member: Lisle Gibbs, PhD Committee member: Theresa Culley, PhD Committee member: Ronald Debry, PhD Committee member: Stephen Matter, PhD 1393 Last Printed:2/24/2011 Document Of Defense Form Historical Specimens Reveal a Century of Genetic Change in Darwin’s Finches By Heather Farrington B.S., University of Mount Union, 1999 A Doctoral Dissertation Submitted to the Faculty of the University of Cincinnati Department of Biological Sciences Advisor: Dr. Kenneth Petren As Partial Fulfillment of the Requirements For the Degree of Doctor of Philosophy in Biology February 2011 ABSTRACT Understanding how populations change through time is critical in the generation of effective conservation biology practices. However, data from multiple time points, especially those that span a significant number of years/generations are rare. In this series of studies, I used a model system, Darwin’s finches of the Galápagos Islands, to investigate questions related to both long term and short term evolution in this system. These species are thought to be in a state of decline due to recent human-induced habitat disturbances, and increasing local extinction events. Darwin’s finches are also well-represented in museum collections. Therefore, this is an ideal system in which to study both change over time and extinction events in fragmented populations. I first used a traditional phylogenetics approach using multiple nuclear introns to examine the overall evolutionary history of this species radiation. These data generated a novel evolutionary tree topology, leading to the reevaluation of the earliest species divergences in this system. I then investigated short term evolutionary trends in warbler finch populations by utilizing genetic information (in the form of microsatellite markers) generated from museum specimens collected approximately 100 years ago. There was no genetic evidence of archipelago-wide population declines in the warbler finches. Both increases and decreases in genetic diversity were noted for individual populations. Decreases in genetic diversity were attributed to fluctuations in population size due to El Niño cycles, while increases were due to migration from other populations. On the island of Española, a suspected case of “genetic rescue”, when a population with low genetic diversity is infused with genetic variation through migration, was revealed. This suggests that migration may play an important role in maintenance of genetic diversity within island populations. Lastly, I again used museum specimens to compare extinct and extant populations to determine if there was any genetic ii indication of population declines prior to extinction events. In this rare test of the predictive ability of standing genetic variation to predict extinction risk, genetic diversity was generally equal to or greater than diversity in populations that have persisted through time. This result emphasizes the caution in using genetic data alone to monitor populations and evaluate extinction risk. All three studies yielded unexpected results, particularly those that utilized museum specimens from natural history collections. The overall conclusion of this dissertation highlights the importance of understanding population interactions in fragmented landscapes, which has major conservation implications for population persistence and viability. iii iv TABLE OF CONTENTS Abstract…………………………………………………………………………………….….…ii Table of Contents……………………………………………………………………………….. v List of Tables and Figures…………………………………………………………….…….…...vi Chapter 1: General Introduction………………………………………………………………...1 Chapter 2: Multi-locus Phylogeny of Darwin’s Finches………………………………………...9 Chapter 3: A Century of Genetic Change and Metapopulation Dynamics in the Galápagos Warbler Finches (Certhidea)……………………………………………………………………40 Chapter 4: Extinction Dynamics in Populations of Darwin’s Finches…………………………86 Chapter 5: General Conclusions………………………………………………...……………..130 v LIST OF TABLES AND FIGURES CHAPTER 2: Table 1: Species and populations included in phylogenetic analysis Figure 1: Map of Galápagos Figure 2: Current phylogenies of Darwin’s finches Figure 3: Maximum likelihood tree for multi-locus intron data set Figure 4: Maximum likelihood tree for multi-locus intron data set including the Cocos Island finch Figure 5: Parsimony tree based on control region data Table S1: Nuclear intron locus information CHAPTER 3: Table 1: Certhidea populations used for cross-temporal analysis Figure 1: Galápagos map indicating islands sampled Figure 2: PCA plots of historic and modern populations Figure 3: Summary genetic data; allelic richness, observed and expected heterozygosity Figure 4: Average inferred population sizes ( = 4Neμ) and immigration rates Figure 5: Historic vs. modern migration rates Figure 6: Percent change over time (allelic richness, migration and population size) Table S1: Museum specimen information Table S2: MSVAR and Bottleneck results Table S3: Table of summary genetic data vi CHAPTER 4: Table 1: Darwin’s finch population sampling information Table 2: Summary genetic data Figure 1: Galápagos map indicating probable extinction events Figure 2: PCA plots of historic and modern populations Table S1: Museum specimen information vii CHAPTER 1: GENERAL INTRODUCTION Understanding the evolutionary dynamics of populations through time is essential for the effective management of biodiversity during this era of increasing human impact in the global ecosystem. Phylogenetic methods have traditionally been used to investigate the evolutionary history of populations and species. These methods typically address long-term evolutionary history and attempt to answer questions related to the timing and sequence of species and population divergences (Avise 2000). This is where my graduate study began, using novel genetic loci to reconstruct the adaptive radiation of Darwin’s finches. Previous studies using various genetic markers have been only marginally successful in resolving the evolutionary history of this group (Petren et al. 1999; Sato et al. 1999, Petren et al. 2005). Although the phylogenetic study was a valuable learning experience, my interests soon shifted to the shorter term evolutionary dynamics of populations and their implications for conservation. Human disturbance is causing population decline and fragmentation of taxa around the world, which has stimulated a need for better understanding of how populations respond to these environmental perturbations. As population sizes decrease and/or fragmentation increases, genetic drift and inbreeding lead to reduced genetic diversity in a population (Wright 1969), limiting the evolutionary potential of a population to adapt to new environmental conditions under natural selection (Fisher 1930). Limited evolutionary potential increases the risk of extinction when environmental conditions change (Gilpin and Soulé 1986). In addition to changes occurring within a single population, as habitat fragmentation becomes more prevalent across landscapes, the evolutionary interactions among populations must also be considered (Wright 1940; Andrewartha and Birch 1954; Levins 1970). Metapopulation studies have demonstrated the importance of gene flow to maintain genetic diversity within individual 1 populations (Hanski and Gaggiotti 2004), and a better understanding of metapopulation dynamics is critical to conservation management efforts in fragmented populations. The majority of our knowledge relating to genetic changes in populations over time is due to experimental and comparative studies that lack a strong temporal component. Experimental studies have been useful in demonstrating inbreeding depression (Willis 1993), genetic drift (Dobzhansky and Pavlovsky 1957), evolution under selection (Mather 1943), and the link between heterozygosity and fitness (Charlesworth and Charlesworth 1999). However, how well these studies translate to wild populations is unclear (Sæther and Engen 2004). Comparative and meta-analysis approaches have been useful in demonstrating reduced genetic diversity in small vs. large populations (Leimu et al. 2006) and endangered vs. non-threatened populations or species (Spielman et al. 2004). Theoretical studies often attempt to extrapolate population changes into the past or future based on current genetic data (Beaumont 1999; Wilson et al. 2003; Kuhner 2006). However, these methods are laden with assumptions related to mutation rates and patterns, population demography and reproductive rates, and mating systems (Excoffier and Heckel 2006), and typically do not account for demographic and environmental stochasticity. The best way to examine genetic evolutionary processes in wild populations is to obtain actual genetic data from the past to track changes through time. However, data from multiple time points, especially those that span a significant number of years/generations are rare. If this data were obtained, it would give us unique insight into the evolutionary dynamics of wild populations and the opportunity to assess how natural populations conform to our understanding of evolutionary processes. Researchers equipped with this

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