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Phylogeography of Selected Southern African Marine Gastropod Molluscs

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Phylogeography of Selected Southern African Marine Gastropod Molluscs EFFECT OF PLEISTOCENE CLIMATIC CHANGES ON THE EVOLUTIONARY HISTORY OF SOUTH AFRICAN INTERTIDAL GASTROPODS BY TINASHE MUTEVERI SUPERVISORS: PROF. CONRAD A. MATTHEE DR SOPHIE VON DER HEYDEN PROF. RAURI C.K. BOWIE Dissertation submitted for the Degree of Doctor of Philosophy in the Faculty of Science at the University of Stellenbosch March 2013 i Stellenbosch University http://scholar.sun.ac.za Declaration By submitting this thesis/dissertation electronically, I declare that the entirety of the work contained therein is my own, original work, that I am the sole author thereof (save to the extent explicitly otherwise stated), that reproduction and publication thereof by Stellenbosch University will not infringe any third party rights and that I have not previously in its entirety or in part submitted it for obtaining any qualification. Date: March 2013 Copyright © 2013 Stellenbosch University All rights resrved ii Stellenbosch University http://scholar.sun.ac.za ABSTRACT Historical vicariant processes due to glaciations, resulting from the large-scale environmental changes during the Pleistocene (0.012-2.6 million years ago, Mya), have had significant impacts on the geographic distribution of species, especially also in marine systems. The motivation for this study was to provide novel information that would enhance ongoing efforts to understand the patterns of biodiversity on the South African coast and to infer the abiotic processes that played a role in shaping the evolution of taxa confined to this region. The principal objective of this study was to explore the effect of Pleistocene climate changes on South Africa′s marine biodiversity using five intertidal gastropods (comprising four rocky shore species Turbo sarmaticus, Oxystele sinensis, Oxystele tigrina, Oxystele variegata, and one sandy shore species Bullia rhodostoma) as indicator species. Sequence data obtained from partial segments of the mitochondrial cytochrome oxidase c subunit 1 (COI), and the nuclear ribosomal DNA (encompassing part of 5.8S, second Internal Transcribed Spacer and part of 28S, hereinafter called ITS2; or comprising part of the first Internal Transcribed Spacer, 5.8S, second Internal Transcribed Spacer and part of 28S, hereinafter called ITS), were used as genetic markers to construct phylogeographic patterns and to investigate demographic histories of the taxa. Population structure was investigated using haplotype network analyses, pairwise ΦST statistics, analysis of molecular variance (AMOVA), isolation by distance analyses, Bayesian analysis of population structure (BAPS) and coalescent analysis of gene flow. Demographic history was analysed through Fu′s Fs tests, mismatch distributions, and Bayesian skyline plots. Demographic analyses suggest that all five intertidal gastropods studied experienced demographic expansions dating to the late Pleistocene. The sandy shore direct developer B. rhodostoma began expansion after the LGM (c. 15 kya) whereas for the four rocky shore broadcast spawners (T. sarmaticus, O. sinensis, O. tigrina, and O. variegata) the onset of expansion coincided with or preceded the LGM (c. 25, 60, 50, 40 kya, respectively). Consistent with recent range expansions and gene flow patterns, the population genetic structure in all species was characterised iii Stellenbosch University http://scholar.sun.ac.za by shallow or a lack of population differentiation. Oxystele variegata was an exception as it showed a deep disjunction, of late Pleistocene origin, between individuals in the west coast Namaqua Bioregion and those in the south coast Agulhas Bioregion. These results provide strong evidence of the vital role that Pleistocene climatic changes and current regimes played in shaping the nature and distribution of biodiversity on the South African coast. In addition, gene flow in all species, except O. tigrina, was remarkably asymmetrical with the regions around Cape Infanta and Port Elizabeth acting as source populations. Considering the generally weak population genetic structure and gene flow patterns detected for most gastropod species studied here, it is recommended that T. sarmaticus, O. sinensis, O. tigrina and B. rhodostoma be managed as panmictic populations, and that the region encompassing Cape Infanta, and Port Elizabeth should be prioritised for conservation as it appears to harbour source populations. Oxystele variegata was the only species showing distinct population structure and in this instance, species specific conservation efforts should recognize this divergence by treating the two genetic assemblages as distinct management units. iv Stellenbosch University http://scholar.sun.ac.za OPSOMMING Historiese vikariante prosesse kan toegeskryf word aan glasiasie, en het tot gevolg gehad dat grootskaalse veranderinge in die omgewing plaasgevind het tydens die Pleistoseen (,012 - 2.6 miljoen jaar gelede, Mjg). Dit het „n beduidende impak gehad op die geografiese verspreiding van spesies, veral ook in die mariene stelsels. Die motivering vir hierdie studie was om nuwe data te voorsien wat sal bydrae tot die voortgesette pogings om die patrone van biodiversiteit langs die Suid-Afrikaanse kus te verstaan. Dit sou ook help om die abiotiese prosesse af te lei wat 'n rol gespeel het in die evolusie van taksa wat in hierdie streek voorkom. Die hoofdoel van hierdie studie was om die effek van die Pleistoseen klimaatsveranderinge op Suid-Afrika se mariene biodiversiteit te bepaal deur gebruik te maak van vyf intergety slak spesies as indikatore (vier wat in rotsagtige gebiede voorkom: Turbo sarmaticus, Oxystele sinensis, Oxystele tigrina, Oxystele variegata en 'n sanderige strand spesies: Bullia rhodostoma). Volgorde data verkry vanaf gedeeltelike segmente van die mitochondriale sitochroom oksidase c subeenheid 1 (COI), en die kern ribosomale DNA (bestaande uit „n deel van 5.8S, tweede interne getranskribeerde spasieërders en 'n deel van 28S), hierna genoem ITS2 is gebruik as genetiese merkers om filogeografiese patrone te dokumenteer en ook om die demografiese geskiedenis van die spesies te ondersoek. Bevolking struktuur is ondersoek deur gebruik te maak van haplotipe netwerk analise, paarsgewyse ΦST statistiek, analise van molekulêre variansie (AMOVA), isolasie deur afstand analise, Bayesiaanse analise van die bevolking struktuur (BAPS) en analise van gene vloei. Demografiese geskiedenis is ontleed deur Fu se Fs toetse, misparing verdelings, en Bayesiaanse luglyn kurwes. Demografiese ontleding dui daarop dat al vyf die intergety slakke wat ondersoek is demografiese uitbreidings ervaar het wat terugdateer tot die einde van die Pleistoseen. Die sanderige strand direkte ontwikkelaar, B. rhodostoma, het die uitbreiding begin na die LGM (c. 15 Kya), terwyl vir die vier rotsagtige kusbewoners wat eiers oor 'n uitgebreide gebiede versprei (T. sarmaticus, O. sinensis, O. tigrina, en O. variegata) het die aanvang van die bevolkings uitbreiding saamgeval met die laaste galsiasie of dit voorafgegaan (c. 25, 60, 50, 40 Kya, onderskeidelik). In ooreenstemming met die onlangse reeks bevolkings uitbreidings, is die bevolking genetiese struktuur in alle spesies gekenmerk deur weinig differensiasie. Oxystele variegata was 'n uitsondering en het 'n ontwrigting van laat Pleistoceen oorsprong getoon tussen individue langs die weskus Namaqua Biostreek en dié in die suid kus Agulhas biostreek. Hierdie resultate voorsien sterk bewyse van die belangrike rol wat die Pleistoseen klimaatsveranderinge gespeel het in die vorming en verspreiding van biodiversiteit langs die Suid-Afrikaanse kus. Daarbenewens, geen vloei in alle spesies, behalwe O. tigrina, was merkwaardig asimmetries. Kaap Infanta en Port Elizabeth verteenwoordig moontlik die bron bevolkings. Met inagneming van die geringe bevolking genetiese struktuur en geenvloei patrone wat waargeneem is vir die meeste slak spesies wat bestudeer is, word dit aanbeveel dat T. sarmaticus, O. sinensis, O. tigrina en B. rhodostoma bestuur word as „n panmiktiese bevolking, en dat die streek wat Kaap Infanta en Port Elizabeth insluit geprioritiseer moet word vir bewaring. Oxystele variegata was die enigste spesie wat duidelike bevolking struktuur getoon het en in hierdie geval, moet spesie spesifieke bewaringspogings aangewend word. v Stellenbosch University http://scholar.sun.ac.za ACKNOLEDGEMENTS First and most importantly I thank my supervisors Professors C.A. Matthee and R.C.K. Bowie, and Dr S. von der Heyden for introducing me to the fascinating field of phylogeography and for their invaluable and insightful guidance throughout my PhD study. I could not have asked for a better supervisory team. I am also indebted to the following people for assisting with sample collection: Dr S. Jackson, Prof S. Daniels, Mr. C. Muller and Miss T. Reynolds. The work was supported by grants from the National Research Foundation (South Africa). I also would like to thank all members of the Evolutionary Genomics Group for being such a wonderful team to work with. I gratefully acknowledge use of facilities on the CBSU computer clusters at the Cornell University Theory Centre for MIGRATE-N analyses. A warm thank you goes to my wife Morleen for her patience and flexibility and for granting me the time and freedom I needed to carry out this work. Finally, a big thank you to my daughters Laura, Tatenda and Lynn for enduring my long hours in the lab and for believing in me. vi Stellenbosch University http://scholar.sun.ac.za CONTENTS Abstract ………………………………………………………….…….....…....…….. iii Opsomming ………………………………………………………………………………..
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