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Phylogeography of the Cellana Limpets of New Zealand: Investigating Barriers to Marine Dispersal and Historical Biogeography

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Phylogeography of the Cellana Limpets of New Zealand: Investigating Barriers to Marine Dispersal and Historical Biogeography Phylogeography of the Cellana limpets of New Zealand: Investigating Barriers to Marine Dispersal and Historical Biogeography Sharyn Jane Goldstien A thesis submitted for the degree of Doctor of Philosophy School of Biological Sciences University of Canterbury, Christchurch New Zealand April 2005 1 Abstract New Zealand is a continental island surrounded by deep-ocean, with a complex system of currents and oceanographic anomalies that may serve to isolate populations of coastal marine organisms. In particular Cook Strait is a 26 km wide body of water separating the North and South Islands which is characterised by complex interactions of tides and converging water masses. Cook Strait is a geologically recent formation that may also impart an historical influence on the biogeographic distribution of coastal marine taxa. In order to investigate the phylogeographic structure of coastal marine taxa around New Zealand’s coastline and to investigate the processes that may contribute toward this genetic structure, I analysed mitochondrial DNA genes from limpet species of the Cellana genus. Phylogenetic analyses of the ribosomal 12S and 16S DNA genes showed that C. ornata may approximate the founding lineage to New Zealand, but these genes were unable to resolve between contrasting biogeographic hypotheses about the origin of Cellana in New Zealand. Intraspecific analyses of the mitochondrial cytochrome b gene from populations throughout the biogeographic range of Cellana ornata, C. radians and C. flava showed concordant genetic discontinuity at Cook Strait. Further analyses suggest that allopatric fragmentation and restricted gene flow have caused significant genetic differentiation between populations of the North and South Island. Demographic expansion was also identified for C. radians. The influence of contemporary nearshore currents and sea surface temperature was assessed using the mitochondrial cytochrome b gene for C. radians and C. ornata. Low levels of genetic differentiation between populations corresponding to ‘current-zones’ suggests that contemporary oceanic processes may be contributing to the genetic pattern observed for these species. However, the shallow divergence between haplotypes and populations restricted thorough investigation of contemporary gene flow. Genealogical concordance across co-distributed marine taxa of New Zealand also lends support to the historic association of genetic and species discontinuities with recent geological changes, such as sea level fluctuations. 2 Acknowledgements During the past four years I have been helped, supported and befriended by many wonderful people, and before I leave anyone out I would like to thank them all. University staff and students, friends, Diamond Harbour locals and Ferry Skippers are all included in my thanks of appreciation. More specifically I would like to thank my supervisors Dave Schiel and Neil Gemmell for their support and guidance; also for encouraging conference participation and collaborative moments. From great leaders are formed great research groups and the Marine Ecology Research Group and the Molecular Ecology Lab are both great groups to be a part of. I am very lucky to have been a part of both of these groups and have enjoyed working and socialising with everyone in them. I am particularly grateful to Bruce Robertson, Victoria Metcalfe and Katherine McBride for setting me up in the laboratory and always being free with advice and providing an ear for troubleshooting. Likewise, the students and post-docs of MERG have always shown enthusiasm for my work and have freely provided assistance, support and of course fun whenever needed. Jack Van Berkel, Nick Etheridge, Linda Morris and Jan McKenzie have been pivotal in making my field and laboratory work successful and indeed feasible. I am particularly grateful to Jack for the many hours he put in to helping me design and create various larval rearing systems at the Edward Percival Field Station in Kaikoura and to Nick for ensuring Summer equipment was ready for Summer. Of course the most laborious of tasks is wading through thesis and publication drafts, and so many thanks are given to Bruce Robertson, Dave Schiel, Dave Taylor, Ian Scott, Janelle Reynolds-Fleming, Mike Hickford, Neil Gemmell and Tammy Steeves for their comments and criticisms on the drafts of my thesis and publication. Finally, I am extremely grateful to the Andrew Mellon Foundation of New York for funding my research. 3 Table of Contents Chapter I General Introduction………………………………………………… 9 1.1 Phylogeography………………………………………………………....10 1.2 Dispersal……………………………………………………………….. 11 1.3 Dispersal Barriers……………………………………………………… 13 1.4 Demographic Disparity………………………………………………… 15 1.5 Phylogeography in New Zealand………………………………………. 17 1.6 Historic New Zealand………………………………………………….. 18 1.7 New Zealand’s Present Oceanic Conditions…………………………… 19 1.8 Colonisation of New Zealand’s Intertidal Zone……………………….. 23 1.9 Cellana…………………………………………………………………. 24 1.10 Thesis Outline………………………………………………………….. 29 Chapter II Molecular Phylogenetics and Biogeography of New Zealand Nacellid Limpets………………………………………………………………… 30 2.1 Introduction…………………………………………………………….. 31 2.2 Methods and Materials………………………………………………… 33 2.2.1 Sample Collection………………………………………………… 33 2.2.2 DNA Preparation…………………………………………………. 34 2.2.3 Analysis…………………………………………………………... 35 2.3 Results…………………………………………………………………. 37 2.4 Discussion……………………………………………………………… 44 Chapter III The Phylogeographic Structure of Cellana limpets of New Zealand: Is Cook Strait a Barrier to Dispersal?................................................................... 46 3.1 Introduction……………………………………………………………. 47 3.2 Materials and Methods………………………………………………… 52 3.2.1 Sample Collection………………………………………………... 52 3.2.2 DNA Preparation…………………………………………………. 54 3.2.3 Sequence Analysis………………………………………………...55 3.2.4 Phylogeographic Structure……………………………………….. 56 3.2.5 Phylogeographic Process…………………………………………. 57 3.3 Results…………………………………………………………………. 58 3.3.1 Sequence Analysis……………………………………………….. 58 3.3.2 Phylogeographic Structure……………………………………….. 61 3.3.3 Phylogeographic Process…………………………………………. 63 3.4 Discussion……………………………………………………………… 66 4 Chapter IV Phylogeography and Dispersal: Are Sea Surface Currents Structuring Marine Populations of New Zealand limpets?................................... 70 4.1 Introduction……………………………………………………………. 71 4.2 Materials and Methods………………………………………………… 77 4.2.1 Sample Preparation………………………………………………. 77 4.2.2 Sequence Analysis……………………………………………….. 78 4.2.3 Phylogeographic Structure……………………………………….. 78 4.2.4 Sea Surface Temperature………………………………………… 79 4.2.5 Migration…………………………………………………………. 79 4.3 Results…………………………………………………………………. 80 4.3.1 Sequence Analysis……………………………………………….. 80 4.3.2 Phylogeographic Structure……………………………………….. 81 4.3.3 Sea Surface Temperature………………………………………… 86 4.3.4 Migration…………………………………………………………. 86 4.4 Discussion……………………………………………………………... 88 Chapter V In Search of Phylogeographic Concordance of New Zealand’s Marine Biota...................................................................................................................... 92 5.1 Introduction……………………………………………………………. 93 5.2 Review of Molecular Studies in New Zealand………………………… 95 5.2.1 Published Literature ……………………………………………… 95 5.2.2 Genetic Homogeneity across taxa..….…………………………… 98 5.2.3 Genetic Discontinuity between the North and South Islands……. 99 5.3 Phylogeographic Concordance………………………………………… 101 5.3.1 Life-history……………………………………………………….. 103 5.3.2 Genetic Discontinuity and Historical Distribution……………….. 106 5.3.3 Biogeographic Concordance……………………………………… 112 5.4 Summary……………………………………………………………….. 116 Literature Cited…………………………………………………………………116 Appendices………………………………………………………………………131 Appendix I – Laboratory Protocols…………………………………………….. 132 A1.1 DNA extraction…………………………………………………… 132 A1.2 Polymerase Chain Reaction reagents, primers and thermal cycle...133 Appendix II – Phylogenetic data………………………………………………...135 Appendix III – Phylogeographic data…………………………………………. 142 A3.1 Population site details…………………………………………………. 142 A3.2 Phylogeographic data………………………………………………….. 144 5 Table of Figures Chapter I General Introduction 1.1 Sea surface currents and continental shelf area around New Zealand………………………………………………………………… 22 1.2 Biogeographic distribution of New Zealand Cellana limpets...……….. 27 Chapter II Molecular Phylogenetics and Biogeography of New Zealand Nacellid Limpets 2.1 Constrained tree topologies for maximum likelihood comparisons.….. 36 2.2 Maximum Parsimony tree of mitochondrial 12S and 16S rRNA……… 39 2.3 Maximum Parsimony tree of combined 12S and 16S data……………. 40 2.4 Maximum Likelihood tree of combined 12S and 16S data………….… 41 2.5 Transition and Transversion plots for 12S and 16S data…………….… 42 2.6 Linearized Neighbour-Joining tree of combined 12S and 16S data…… 43 Chapter III The Phylogeographic Structure of Cellana limpets of New Zealand: Is Cook Strait a Barrier to Dispersal? 3.1 Study sites sampled around New Zealand…………………………….. 53 3.2 Haplotype networks and shared haplotype distributions for C. ornata, C. radians and C. flava……………………………………... 60 3.3 MDS plots of dXY for C. ornata, C. radians and C. flava……………... 61 3.4 Mismatch Distributions for C. ornata and C. radians…………………. 64 3.5 Haplotype networks and NCA design for C. ornata, C. radians and C. flava………………………………………………………………… 65 Chapter IV Phylogeography and Dispersal: Are Sea Surface Currents Structuring Marine Populations of New Zealand limpets? 4.1 Currents
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