Adaptations in Allopatric Populations of Triakis Megalopterus Isolated by the Benguela Current

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Adaptations in Allopatric Populations of Triakis Megalopterus Isolated by the Benguela Current Adaptations in allopatric populations of Triakis megalopterus isolated by the Benguela Current. Steps towards understanding evolutionary processes affecting regional biodiversity. A thesis submitted in fulfilment of the requirements for the degree of DOCTOR OF PHILOSOPHY at RHODES UNIVERSITY by Michelle Soekoe February 2016 Abstract This study was initiated to gain a better understanding of evolution and adaptation of elasmobranchs by investigating how a putative biogeographic barrier, the Benguela Current, had influenced populations of a demersal shark species, Triakis megalopterus. It was hypothesized that the Benguela Current formed a biogeographic barrier in the distribution of T. megalopterus and was responsible for the divergence between South African (SA) and Angolan (AN) populations. Since elasmobranchs are generally characterized by a slow rate of evolutionary change and conservative morphology and life history traits, it was hypothesized that there would be limited genetic, morphological and life history divergence between the populations. Both mtDNA Control Region (mtCR) and microsatellites (nDNA) were used to assess population connectivity and structure of T. megalopterus. The mtCR predominantly showed a northern (Angola, AN, and Namibia, NA) versus southern (Western Cape, WC, and Eastern Cape, EC) Benguela subsystem arrangement. This suggested that the formation of the Benguela Current had an influence on the genetic structure of T. megalopterus during the early Pleistocene. The nDNA, however, showed a distinct transoceanic, Atlantic (AN, NA, WC) versus Indian Ocean (EC) arrangement, and this was attributed to the more recent exposure of the Agulhas Bank and reduced rocky shore habitat during the glaciations of the late Pleistocene. Traditional morphological analyses on full body and tooth morphology were used to assess phenotypic plasticity and/or adaptability of T. megalopterus. A novel method of geometric morphology, with potential for non-lethal application, was developed and tested to examine interpopulation divergence in shape. Traditional morphometrics showed significant divergence between populations and this variation was congruous with the mtCR haplotypes. However, the divergence in the truss variables was not concomitant to the haplotypes and i suggested that differences in shape may be attributed to phenotypic plasticity. There was limited divergence in the tooth morphology between populations. The divergence in several morphological characters associated with swimming speed and manoeuvrability may be attributed to both habitat structure and dominant prey in the different biogeographic zones. The diet of T. megalopterus consisted primarily of crustaceans, teleosts and molluscs. The significant variation in the diet between populations suggested a generalist tooth configuration and broad trophic adaptability. There was significant divergence in the interpopulation life history parameters. The AN population had the fastest growth, smallest size at maturity, and shortest longevity. Individuals in the EC population had the youngest age at maturity, while the WC population had the earliest parturition. This divergence may be attributed to the contrasting thermal regimes in the three biogeographic regions and the dissimilar exploitation rates of the three populations. The results of this thesis demonstrated that a combination of the formation of the Benguela Current and sea level change most likely contributed to vicariance of three populations of T. megalopterus. The significant interpopulation morphological and life history divergence appeared to be both phenotypic and genetic, and suggested that contrasting environmental drivers can result in relatively rapid change in elasmobranchs. ii "The sea, once it casts its spell, holds one in its net of wonder forever." ~Jacques Yves Cousteau~ iii Acknowledgements I would like to express my extreme gratitude to the following people and organizations; without all of you, this project would never have been possible. Warren and Malcolm: without you providing me with the opportunity to tackle this project, my dream to do “sharky” science may never have come true. Thank you for the support and guidance. Your vast knowledge and analytical thinking always has me in awe. Thanks to you, I have gained immeasurable experience in a vast array of research, and I’ve been blessed to visit the most incredible places while doing it. The National Research Foundation: for the financial support during my PhD and Department of Agriculture, Fisheries and Forestry for the permits for this research. The incredible Flamingo Lodge in southern Angola: thank you for all of your support and sharing your little piece of paradise with me, what a magical place. Aletta, Simo and Daphne (Department of Genetics at Stellenbosch University): thank you for taking me under your wings. You achieved the impossible, you taught me all about genetics AND made sure I enjoyed every minute of it. Taryn Bodill from the South African Institute for Aquatic Biodiversity: for all of your patience and guidance in the laboratory with my mtDNA. My fellow post-graduates, Alexander Winkler, Chenelle De Beer and Roy Bealey: you were my fisherman, scribes, assistant dissectors, teachers, entertainers and, at times, even my slave drivers. Thank you for all of your help, even when we were all exhausted; you always stuck it out until the last specimen was processed. To Nic: thank you for putting up with me through all of the thesis stress. The looooong hours, late nights and early morning, it’s finally all over. I love you. Last, but certainly not least, my parents: for supporting me in the pursuit of my dream, even when it meant giving up a great career to go back to the books. I will always be eternally grateful for the endless love, support, encouragement and motivation. Thank you both for giving me the strength and the opportunity to reach for the stars and chase my dreams. Granny, my biggest supporter, I did it! NOW you can pop the champagne. iv Table of contents Abstract ........................................................................................................................................ i Acknowledgements ................................................................................................................... iv List of tables .............................................................................................................................. ix List of figures ............................................................................................................................ xi Chapter 1: General introduction ................................................................................................ 1 Thesis outline ........................................................................................................................ 10 Chapter 2: Site selection and general methods ........................................................................ 12 Study sites ............................................................................................................................. 12 Southern Angola ............................................................................................................... 12 Northern/Central Namibia ................................................................................................ 14 Western Cape, South Africa ............................................................................................. 15 Eastern Cape, South Africa .............................................................................................. 15 General material and methods .............................................................................................. 16 Chapter 3: Genetic connectivity of Triakis megalopterus across its southern African distribution ................................................................................................................................ 18 Introduction ........................................................................................................................... 18 Material and methods ............................................................................................................ 23 Sample collection and DNA extraction ............................................................................ 23 Species identification ........................................................................................................ 24 mtCR sequencing and alignment ...................................................................................... 24 mtCR sequence analysis ................................................................................................... 25 Population demographics ................................................................................................. 25 Microsatellite genotyping ................................................................................................. 26 Marker validity ................................................................................................................. 28 Genetic diversity and population differentiation .............................................................. 29 Demographic history ........................................................................................................ 29 v Results and interpretation ..................................................................................................... 30 Mitochondrial DNA (mtCR)
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