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ROYAL HOLLOWAY UNIVERSITY of LONDON School of Biological Sciences INFLUENCE of the BENGUELA CURRENT in GENETIC SUB-STRUCTURING O

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ROYAL HOLLOWAY UNIVERSITY of LONDON School of Biological Sciences INFLUENCE of the BENGUELA CURRENT in GENETIC SUB-STRUCTURING O ROYAL HOLLOWAY UNIVERSITY OF LONDON School of Biological Sciences INFLUENCE OF THE BENGUELA CURRENT IN GENETIC SUB-STRUCTURING OF COMMERCIALLY EXPLOITED FISH SPECIES by Romina Paula Novo Lopes Henriques Thesis submitted as part of the requirements for the awarding of the degree of Doctor of Philosophy November 2011 Declaration of Work I, Romina Paula Novo Lopes Henriques, hereby declare that all the work presented in this thesis is from my authorship, with the exception of the laboratory techniques employed to isolate microsatellite markers (described in Chapter 2.2.4) that were performed by my colleague Dr Niall McKeown. Name: Date: 18th November 2011 2 Acknowledgments The present work would not have been possible without the valuable help of numerous people throughout these last 4 years. First, and foremost, I would like to thank my supervisor, Paul Shaw, for giving me the opportunity to study such fascinating oceanographic system and its impact on species evolution. Thank you for all the help, guidance and insightful comments that made me learn so much. Also, I would like to thank the Portuguese FCT (Fundação para a Ciência e Tecnologia) that funded this work through a PhD scholarship (SFRH/BD/36176/2007). This work would not have been the same without the never-ending efforts of Warren Potts and Warwick Sauer. I owe you many of my samples, a lot of my knowledge on life history, and amazing field trips to southern Angola that made my life happier. Thank you as well to my colleagues: Yoko, Niall, Olgaç and Janek. Your help was very much appreciated in times of trouble and despair. Thank you to the “ancient DNA” people: Ian Barnes, Selina Brace, Jessica Thomas and Peter Heintzman that helped me innumerous times throughout this thesis and provided invaluable conversations about the evolution of species. In Angola, I would like to thank Prof. Carmen Santos (Universidade Agostinho Neto – Luanda), the Flamingo and Cunene River Mouth Lodge people, Paulo Carqueja, Cabeça, Tim, and Jerry, and the fishing companies Pesca Sede and Sicopal for all the help, all the consideration and all the efforts that made my fieldtrips easier. Especially, I would like to thank my uncles Manuel and Cassiano Henriques, and cousins Jaime and Elizabeth Novo that took me in, fed me and helped me get to some dodgy places to collect fins at the most unearthly hours. I will never forget all that you have done. In addition, some of the samples used in this work were collected by local collaborators, to who I am deeply grateful: Tiago Peixoto (Diplodus spp); Nuno Prista (A. regius); 3 João Pereira (D. vulgaris); Spyker (A. inodorus); Michael Steer (A. japonicus), and Alejandro de Vera Hernández (A. aequidens). Finally, to all my friends (that are too many to name) that helped me through this journey and kept me sane. Also, many, many thanks to Nuno, for the patience and love, and my family (mom, dad, sis’) that stayed by me, and endured hours of random babbling about fish. I love you all very much. 4 Abstract Oceanographic features such as currents, fronts and upwelling cells have been recognised as possible factors driving population differentiation within species. The Benguela Current is one of the oldest upwelling systems in the world, located off the west coast of Southern Africa, and represents a biogeographical boundary between the Atlantic and Indo-Pacific Oceans. Previous studies have reported the influence of this system in isolating several marine taxa between the two oceans. However, few have been conducted within the Benguela Current boundaries, in order to understand its role in shaping population genetic structure of fish species at a regional level. The present study documents the influence of the Benguela Current oceanographic features on the genetic differentiation, population connectivity and evolutionary history of five coastal fish species (Diplodus capensis, Argyrosomus inodorus, Argyrosomus coronus, Atractoscion aequidens and Lichia amia), and one oceanic pelagic fish species (Thunnus albacares). Results for both mitochondrial and nuclear marker variation in all coastal species revealed a similar geographical pattern of population genetic structuring despite distinct differences in life history features. The oceanic species exhibited shallow population differentiation between Atlantic and Indian Oceans. For coastal species, different depths of differentiation were observed, ranging from speciation events (A. aequidens, A. coronus and A. japonicus) to shallow structuring (A. inodorus and T. albacares). Furthermore, in these cases, population structures were coincident with the Benguela Current oceanographic features, suggesting that the system may represent a vicariant barrier to dispersal of coastal fish species. Congruence between mitochondrial and nuclear markers suggests that population isolation was not a single historical event, but has persisted over large timescales and is still active. The existence of cryptic speciation events, and the high levels of genetic diversity and differentiation documented make the Benguela Current a natural laboratory to study evolutionary mechanisms shaping biodiversity and genetic population structure of marine fish species. 5 Table of Contents Declaration of Work 2 Acknowledgments 3 Abstract 5 Table of Contents 6 List of Tables 10 List of Figures 17 INTRODUCTION 23 CHAPTER 1: Introduction and State of the Art 24 1.1. The Benguela Current 24 1.1.1. Oceanographic features 24 1.1.2. Changes in the Benguela Current through time 29 1.1.3. The Benguela ecosystem 31 1.2. Population genetics and evolutionary history of marine species 33 1.2.1. Population genetics in marine species: principles and general concepts 33 1.2.2. Molecular markers 34 Mitochondrial DNA and nuclear DNA sequences 35 Microsatellites 36 1.2.3. Usefulness of molecular markers in fisheries management 38 1.3. Influence of oceanographic features in marine fish population structure 40 1.4. The study species 43 1.4.1. Diplodus capensis (Smith, 1844) - Blacktail 44 1.4.2. Argyrosomus spp. 46 Argyrosomus coronus Griffiths & Heemstra 1995 – West coast dusky kob 46 Argyrosomus inodorus Griffiths & Heemestra 1995 – Silver kob 47 Argyrosomus japonicus (Temminck & Schlegel, 1843) – Dusky kob 48 1.4.3. Atractoscion aequidens (Cuvier, 1830) - Geelbeck 49 1.4.4. Lichia amia (L. 1758) - Leerfish 51 1.4.5. Thunnus albacares (Bonnaterre, 1890) – Yellowfin tuna 51 1.5. Aims and objectives 53 METHODS 55 CHAPTER 2: General Methodology 56 6 2.1. Sampling 56 2.2. Molecular techniques 58 2.2.1. DNA extraction 58 2.2.2. PCR amplification and sequencing of mitochondrial and nuclear DNA loci 58 2.2.3. Amplification and screening of microsatellite DNA markers 60 Diplodus capensis 60 Argyrosomus coronus / A. inodorus 61 Thunnus albacares 61 Atractoscion aequidens 62 2.2.4. Isolation of 12 microsatellite markers for Atractoscion aequidens (Cuvier, 1830), Sciaenidae: an overexploited marine fish 63 2.3. Statistical analyses 66 2.3.1. Mitochondrial DNA 66 Population structure and phylogeographic patterns 66 Evolutionary history 67 2.3.2. Microsatellites 70 Population structure 70 Demographic history 71 RESULTS 73 CHAPTER 3: Diplodus capensis 74 3.1. Population structure and evolutionary history of Diplodus capensis (Smith 1844) in a heterogeneous environment: the Benguela Current 74 3.1.1. Introduction 74 3.1.2. Methods 76 3.1.3. Results 80 3.1.4. Discussion 91 CHAPTER 4: Argyrosomus spp. 101 4.1. Tempo and mode of evolution of Argyrosomus spp. (Percifomes, Sciaenidae) in the eastern Atlantic: evidence of Pleistocene origins 101 4.1.1. Introduction 101 4.1.2. Methods 103 4.1.3. Results 106 4.1.4. Discussion 115 7 4.2. First evidence of climate-induced shifts in dominant species in the Benguela Current: Argyrosomus coronus and Argyrosomus inodorus 123 4.2.1. Introduction 123 4.2.2. Methods 125 4.2.3. Results 129 4.2.4. Discussion 134 4.3. Evolutionary history of Argyrosomus coronus (Perciformes: Sciaenidae) in a highly unstable oceanographic system, the Angola-Benguela Front 141 4.3.1. Introduction 141 4.3.2. Methods 143 4.3.3. Results 147 4.3.4. Discussion 156 CHAPTER 5: Atractoscion aequidens 163 5.1. Population structure and evolutionary history of Atractoscion aequidens (Cuvier, 1830) across the Benguela Current region 163 5.1.1. Introduction 163 5.1.2. Methods 164 5.1.3. Results 167 5.1.4. Discussion 175 5.2. Marine population evolution across the Benguela Current system: molecular evidence for allopatric speciation in a Sciaenid fish, Atractoscion aequidens (Cuvier 1830) 183 5.2.1. Introduction 183 5.2.2. Methods 185 5.2.3. Results 188 5.2.4. Discussion 194 CHAPTER 6: Lichia amia 200 6.1. Population structure and evolutionary history of a coastal pelagic fish in the Benguela Current: Lichia amia (L.1758) 200 6.1.1. Introduction 200 6.1.2. Methods 201 6.1.3. Results 203 6.1.4. Discussion 207 CHAPTER 7: Thunnus albacares 211 8 7.1. Population and phylogeographic structuring of Thunnus albacares (Bonnaterre, 1788) around southern Africa: implications for fisheries management and conservation 211 7.1.1. Introduction 211 7.1.2. Methods 213 7.1.3. Results 217 7.1.4. Discussion 225 DISCUSSION 231 CHAPTER 8: General Discussion and Conclusions 232 8.1. Limitations of the present work 232 8.1.1. Sampling 233 8.1.2. Markers and statistical analyses 233 8.2. Contributions to the knowledge of genetic population sub-structuring of marine species 235 8.2.1. Genetic diversity and population structure of the study species 235 8.2.2. Comparison of patterns of genetic diversity between the Benguela Current and other oceanographic systems of the world 242 8.3. Contributions to the knowledge of evolutionary and demographic history in marine species 244 8.3.1. Evolutionary history of the study species 244 8.3.2. Demographic history of the study species 248 8.4.
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