THE UNIVERSITY of HULL Genetic Factors Affecting Establishment
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THE UNIVERSITY OF HULL Genetic factors affecting establishment during invasions: the introduction of the topmouth gudgeon (Pseudorasbora parva) and the rainbow trout (Oncorhynchus mykiss) in Europe being a Thesis submitted for the Degree of Doctor of Philosophy in the University of Hull by Andrea Simon MSc July 2012 i Abstract The study of biological invasions is a major research topic, both because of the ecological and economical damage caused by invasive species and also as a great natural experiment to study evolutionary responses of non-native populations to their new environment, and the factors influencing invasions. Introduced species often evolve rapidly, despite the assumed loss of genetic variation associated with bottlenecks during the invasion process. In order examine the processes and mechanisms affecting the outcome invasions I studied two non-native fish species, the topmouth gudgeon (Pseudorasbora parva) is an Asian cyprinid that is found in most European countries as a result of accidental introductions. Rainbow trout (Oncorhynchus mykiss) has been introduced from the United States for aquaculture and angling, however, despite numerous introductions, it has only been able to establish in few European waters. I used mitochondrial DNA and microsatellite markers to understand the invasion history of these species and the factors that influence their establishment success/failure. Part of the cytochrome b gene was analysed in European and native Asian P. parva populations and microsatellite markers were used to investigate the source populations of the species. The analyses elucidated the colonisation pattern of P. parva in Europe and supported the hypothesis that the species spread through long-distance and stepping-stone methods and originate from admixed source populations. ii In O. mykiss, part of the d-loop region of the mitochondrial genome was analysed to compare the phylogeographic structure of native US and introduced European populations to examine the spread of the species outside its native range, as well as to find out whether the resistant Hofer strain is the source population of the European rainbow trout populations. I found that European populations are likely to originate from various sources, mainly from California. The Hofer strain is likely to have contributed to some of the wild European populations. Assessing the role of these processes is fundamental in understanding invasive species and finding suitable management practices to control them. From an evolutionary point of view, I was able to detect some of the processes that are important during invasions, in these studies particularly the role of multiple introductions and introduction from genetically admixed source populations. iii Acknowledgements I am extremely grateful to my supervisors, Dr. Bernd Hänfling, Dr. Cock van Oosterhout and Dr. Lori Lawson-Handley for their advice and support throughout my studies and I would like to thank them for their comments and suggestions for my thesis and to Dr. Bill Hutchinson for his help with my work. My parents and family have always encouraged me (köszi drága Anyucikám, kérek mákostésztát!) and a big thank you to my girls, Kat, Eda, Manci, Krinya, Isabel, Violaine, Caitriona, Sandra - could not have done it without the chats and countless phonecalls, I am very lucky to have such great family and friends. Thanks to my extended family, Nancy and Kenneth Stuart for letting their house be my home away from home...and for the G&Ts. In my daily work, I have been very fortunate to be part of the Evolutionary Biology Group in Hull - what a great group to work in, thank you everyone! I would also like to thank NERC for funding my work and the many people who helped me with samples or advice: Professor Robert Behnke and Mrs Sally Behnke, Susan Rivers, Péter Takács, Gary Kelley, Kevin Gadsby, Eva Zahorska and Stephen Moores. I am also grateful to my examiners, Dr. Stefano Mariani and Dr. Domino Joyce for reading and commenting on my thesis, thank you! iv Declaration I declare that this thesis has been compiled by myself and is the result of my own investigations. It has not been submitted for any other degree, and all other sources of information have been duly acknowledged. Andrea Simon v Contents CHAPTER I: General introduction 1.1 Introduction: Biological invasions 1 1. 1. 2 The history of invasion biology 3 1. 1. 3 Stages of the invasion process 4 1. 1. 4 Factors facilitating the invasion process 5 1. 1. 5 Evolutionary aspects of invasions 7 1. 2 Population genetic approaches to study biological invasions 11 1.2.1 History of population genetics and theoretical background 11 1.2.2 Genetic markers 13 1.2.2.1. Mitochondrial DNA 13 1.2.2.2. Microsatellite markers 16 1.2.3 Developments in population genetics 18 1.3 Study species 20 1.3.1 Rainbow trout (Oncorhynchus mykiss) as a study species 20 1.3.1.1 Life history of the species 20 1.3.1.2 The evolutionary history of the rainbow trout 23 1.3.1.3 Genetics of the rainbow trout 26 1.3.1.4 Aquaculture 26 1.3.1.5 The Hofer strain 27 1.3.1.6 The Wye population 28 1.3.2 Topmouth gudgeon (Pseudorasbora parva) as a study species 29 1.3.2.1 Life history of P. parva 29 1.3.2.2 Control of the species 30 vi 1.4 Aims and Objectives 32 CHAPTER II: Invasive cyprinid fish in Europe originate from the single introduction of an admixed source population followed by a complex pattern of spread 2.1. Introduction 35 2.2 Materials and methods 38 2.2.1 Sampling scheme and hypothesis testing 38 2.2.2 Molecular procedures 44 2.2.3 Phylogenetic analyses and haplotype network 44 2.2.4 Population genetic data analysis 46 2.2.5 Approximate Bayesian Computation (DIY ABC) 48 2.3. Results 49 2.3.1 Phylogenetic and network analysis and distribution of haplotypes 49 2.3.2 Diversity within populations 53 2.3.3 Genetic differentiation and population structure 57 2.3.4 Approximate Bayesian Computation (DIY ABC) 59 2.4. Discussion 63 2.4.1 Population genetics of native populations 63 2.4.2 Colonisation history 66 2.4.3 Evidence of hybridisation 69 2.5. Conclusion 69 vii CHAPTER III: Understanding the spread and invasion history of topmouth gudgeon (Pseudorasbora parva) populations in Europe based on microsatellite data analysis 3.1 Introduction 71 3.2 Materials and Methods 74 3.2.1 Sampling Scheme and laboratory procedures 74 3.2.2 Data analysis 77 3.3 Results 80 3.4 Discussion 89 3.4.1 Genetic signal of invasion history 89 3.4.2 Evidence for multiple invasions of P. parva in the UK 92 3.4.3 What facilitates successful invasion? 93 3.4.4 Incongruence between markers 94 3.5 Conclusion 94 CHAPTER IV: Mitochondrial DNA analysis of population structure of rainbow trout (Oncorhynchus mykiss) in its native and introduced range 4.1 Introduction 96 4.2 Materials and Methods 101 4.3 Results 105 4.4 Discussion 116 viii CHAPTER V: General discussion 5.1 Summary of findings 123 5.1.1 mtDNA analysis in P. parva 123 5.1.2 Microsatellite analysis of European P. parva Populations 123 5.1.3 mtDNA analysis of O. mykiss in its native and introduced range 124 5.2 General discussion 125 5.2.1 Introduction 125 5.2.2 P. parva introductions 126 5.2.3 P. parva introductions in Europe 128 5.2.4 O. mykiss introductions 129 5.2.5 Hybridization 131 5.2.6 Incongruence between the markers 132 5.2.7 Future genetic studies 132 5.3 Final conclusions and future work 137 References 136 ix CHAPTER I General introduction 1.1 Introduction: Biological invasions Many populations change their range distribution naturally over time. However, substantial natural range shifts usually take place over geological time scales and sudden natural expansions are rare events. In contrast, human mediated dispersal during the last two centuries has led to large-scale species translocations resulting in increased levels of biotic homogenisation across continents. Species that are introduced by humans either intentionally or unintentionally to geographic areas where they do not naturally occur are defined as Non- Indigenous Species (NIS) (Delach 2006; Shigesada and Kawasaki 1997). Only those NIS that establish populations in the non-native area and spread outside a human-dominated environment, are considered to be invasive (Levine, 2008). Biological invasions are a constant ecological threat and are now considered to be the second most important cause for the loss of biodiversity after habitat loss (Sala et al 2000). Apart from the ecological costs, non-native species have been associated with extremely high economic costs: in the United States the cost of invasive species in the past few years on average were estimated to be around $137 billion per year (Pimentel et al 2000) and vary greatly between taxa (Figure 1). Human activities, such as travelling, worldwide commerce between countries continue to increase, and these activities are greatly encouraging and promoting the spread of non-native species. As the number of invasive species continues to increase, predicting invasions has become more 1 relevant in research. Consequently, understanding the effects of biological invasions and comprehending the mechanisms supporting the invasion process is an increasingly important area of research. The study of invasive species is emerging as a new biological discipline and research area (Davis 2009) and has developed into a subfield within ecology (Lodge 1993) with its own theoretical and conceptual framework. In invasion biology theory it is widely accepted that only a small proportion of invasive species become established in the new environment.