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Phylogeographic Patterning of Three Co-Distributed Forest-Dwelling Reptile Species Along the East Coast of South Africa

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Phylogeographic patterning of three co-distributed forest-dwelling reptile species along the east coast of South Africa By Theo Busschau Thesis presented in partial fulfilment of the requirements for the degree Master of Science in Zoology at Stellenbosch University Supervisor: Prof. Savel R. Daniels Co-supervisor: Mr. Werner Conradie Faculty of Science Department of Botany and Zoology December 2019 Stellenbosch University https://scholar.sun.ac.za Declaration By submitting this thesis electronically, I declare that the entirety of the work contained therein is my own, original work, that I am the authorship owner thereof (unless to the extent explicitly otherwise stated) and that I have not previously in its entirety or in part submitted it for obtaining any qualification. December 2019 Copyright © 2019 Stellenbosch University All rights reserved II Stellenbosch University https://scholar.sun.ac.za Abstract This study investigates the phylogeographic structure of three co-distributed forest-living reptile species, the Pondo flat gecko (Afroedura pondolia), the forest thread snake (Leptotyphlops sylvicolus) and the Natal black snake (Macrelaps microlepidotus), by sampling specimens from the Eastern Cape and KwaZulu-Natal provinces of South Africa. Phylogenetic results, using Bayesian inferences and maximum likelihood, from the combined mitochondrial sequence data (ND4 and cyt b), along with population genetic analyses suggest the presence of broadly congruent biogeographic breaks among the study taxa. Sequence divergence values suggest that A. pondolia and L. sylvicolus represent species complexes comprising several cryptic species while M. microlepidotus exhibits population level differentiation. Divergence-time estimates indicate that cladogenesis within the study taxa occurred during the late Miocene to the Plio/Pleistocene climatic shifts, suggesting that cladogenesis was driven by climatic oscillations and suitable habitat fragmentation. We further investigate the species level divergence within A. pondolia and L. sylvicolus by including two partial nuclear loci (PRLR and RAG1) and employing several species delimitation methods (ABGD, bGMYC, PTP and STACEY). The species delimitation results were generally incongruent, estimating between two and 14 species nested within A. pondolia and between ten and 12 species nested within L. sylvicolus. In both taxa, the species hypotheses retrieved by STACEY based on the total-evidence data were preferred and used to define groups in the morphological analyses. In A. pondolia the multivariate morphological analyses indicate statistically significant differences among the four putative species, corroborating the presence of four species. In L. sylvicolus the morphological analyses exhibit large overlap among the ten putative species but indicate differences between grassland and forest species. The narrow distributions of the putative species identified in the present study have further implications for the conservation status of A. pondolia and L. sylvicolus and suggest that the fragmented forest habitat along the east coast of South Africa may harbor significantly higher levels of diversity than currently recognized. III Stellenbosch University https://scholar.sun.ac.za Acknowledgements I would like to thank my supervisors, Prof. Savel R. Daniels and Werner Conradie, for providing me with this opportunity and for their guidance and support throughout the project. The following people and institutions are thanked for assisting with field work and/or providing additional material: Tyrone Ping, Alex Rebelo, Luke Kemp, Chad Keates, Adriaan Jordaan, Courtney Hundermark, Richard Mckibbin, Shelley Edwards, Anthony Howes, Amy Panikowski & Gareth Coleman, Andrew MacLeod, Trent Fairley, Raeleen van Schalkwyk, Leigh Richards (Durban Natural Science Museum), Mary & Kevin Cole (East London Museum), Sharlene van der Slikke, Callum & Shaun Bayman, Chris Hobkirk (Lowveld Venom Suppliers), Terrence Whittle (Pure Venom), Juan Marillier (The Venom Pit), Pieter Potgieter, Ian Taylor, Judith Kushata, Emmanuel Matamba, Evelyn Raphalo, Jake Mulvaney and Monika Moir. The Foundational Biodiversity Initiative Program (FBIP) and National Research Foundation (NRF) are thanked for funding the Eastern Cape Forest Research project (grant number: 98871) and providing a bursary. Jan Venter, Brian Reeves and Eastern Cape Parks and Tourism Agency (ECPTA) are thanked for supporting and funding fieldwork to the ECPTA Nature Reserves. The Central Analytical facility of the University of Stellenbosch is thanked for DNA sequencing. Ilze Boonzaaier is thanked for producing the maps. Collection permits were provided by the Department of Economic Development, Environmental Affairs and Tourism (Permit numbers WIFM 09-2017 and WIFM 04-2016) and Ezemvello KZN Wildlife (Permit number OP4101/2017). IV Stellenbosch University https://scholar.sun.ac.za Table of contents Declaration .......................................................................................................................... II Abstract .............................................................................................................................. III Table of contents ................................................................................................................ V List of tables ...................................................................................................................... VII List of figures ................................................................................................................... VIII List of appendices ............................................................................................................. XI Chapter 1. General introduction ........................................................................................ 1 Chapter 2. Evidence for cryptic diversification in a rupicolous forest-dwelling gecko (Gekkonidae: Afroedura pondolia) from a biodiversity hotspot ...................................... 7 2.1 Introduction ................................................................................................................... 7 2.2 Materials and Methods ................................................................................................ 10 2.2.1 Sample collection ................................................................................................ 10 2.2.2 DNA sequencing ................................................................................................. 13 2.2.3 Phylogenetic analyses ........................................................................................ 14 2.2.4 Divergence-time estimates .................................................................................. 14 2.2.5 Population genetic analyses ................................................................................ 15 2.2.6 Species delimitation ............................................................................................ 15 2.2.7 Morphological analyses ....................................................................................... 17 2.3 Results ......................................................................................................................... 18 2.3.1 Mitochondrial DNA tree topology and divergence-time estimation ....................... 18 2.3.2 Total DNA evidence tree topology ....................................................................... 21 2.3.3 Population genetic analyses ................................................................................ 23 2.3.4 Species delimitation ............................................................................................ 24 2.3.5 Morphological analyses ....................................................................................... 27 2.4 Discussion ................................................................................................................... 31 V Stellenbosch University https://scholar.sun.ac.za Chapter 3. Phylogeographic patterning of two co-distributed fossorial forest-living snake species reveals hidden diversity .......................................................................... 46 3.1 Introduction ................................................................................................................. 46 3.2 Materials and Methods ................................................................................................ 49 3.2.1 Sample collection ................................................................................................ 49 3.2.2 DNA sequencing ................................................................................................. 54 3.2.3 Phylogenetic analysis .......................................................................................... 55 3.2.4 Divergence-time estimates .................................................................................. 56 3.2.5 Population genetic analyses ................................................................................ 56 3.2.6 Species tree and species delimitation in L. sylvicolus .......................................... 57 3.2.7 Morphological analyses of L. sylvicolus ............................................................... 58 3.2.8 Alternative phylogenetic hypotheses ................................................................... 59 3.3 Results ........................................................................................................................
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