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Detecting a Signature of Adaptive Radiation: Diversification in Lake Tanganyika Catfishes

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Detecting a signature of adaptive radiation: diversification in Lake Tanganyika catfishes Claire Rachel Peart University College London A thesis submitted for the degree of Doctor of Philosophy September 2014 UCL Department of Genetics, Evolution and Environment Declaration I, Claire Rachel Peart, confirm that the work presented in this thesis is my own. Where information has been derived from other sources, I confirm that this has been indicated in the thesis. Claire Rachel Peart Candidate Statement of authorship Chapter 2 has been published in Molecular Phylogenetics and Evolution with co- authors Julia Day, Roger Bills and Mark Wilkinson (Appendix 4). I collected and analysed the data and wrote the first draft of the manuscript. Comments from co- authors were incorporated into the text prior to publication. I took part in a field trip to the Zambian portion of Lake Tanganyika to collect specimens and tissues samples for stable isotope analysis and DNA sequencing used in Chapters 2 - 5. I carried out the majority of the lab work, though some extractions and PCRs for Chapter 2 were carried out with the assistance of a lab technician, Mari-Wyn Burley (UCL). Sanger sequencing was also performed by Mari-Wyn Burley at UCL. Illumina sequencing and RAD-seq library quantification was performed by the FAS Center for Systems Biology, Harvard University. 199 unpublished sequences prepared in the laboratory of Dr Thomas Near are used in Chapter 4. I assembled and aligned all sequence data, and performed all analyses. Stable isotope analyses (Chapter 4) were carried out at the Scottish Universities Environmental Research Centre (SUERC), Life Sciences Mass Spectrometry Facility. I prepared and measured all samples and received training from Jason Newton (SUERC) to run the samples on the mass spectrometer. Morphological data for 303 Synodontis specimens in Chapter 5 were collected jointly by Julia Day and I including specimens from both the Royal Museum of Central Africa, Tervuren and the Natural History Museum, London. I collected data for the remaining 309 specimens in Chapter 5 and all specimens used in Chapter 4 alone. 2 Abstract This thesis compares two independent radiations of catfish in Lake Tanganyika, Claroteine and Synodontis catfishes, to investigate generalities in patterns and processes of diversification between radiations in an ancient “island-like” environment. The introductory chapter places this work in a theoretical context and explores previous research on taxa from Lake Tanganyika. Chapter two provides the first molecular phylogeny of species in the sub-family Claroteinae from Lake Tanganyika, including additional putative species of the genus Phyllonemus. This phylogeny is fossil calibrated to assess when diversification occurred and molecular species delimitation is also performed. Chapter three investigates geographic structure in one species from each radiation, Lophiobagrus cyclurus (from the Claroteine radiation) and Synodontis multipunctatus. Each species was sampled from multiple localities along the length of Lake Tanganyika and their DNA sequenced using restriction site associated (RAD) sequencing to produce large genomic datasets. These datasets allow the comparison of geographic patterns between taxa and, in the Lophiobagrus dataset (which also includes the closely related species L. aquilus), an investigation into the extent of introgression. Chapter four investigates niche partitioning and morphological diversification in both the claroteine and Synodontis radiations. These analyses are conducted using a single dated molecular phylogeny containing both of the radiations allowing explicit comparisons. Eco-morphological divergence is assessed using both morphological measurements thought to be ecologically relevant (e.g., size of the eye) and stable isotope ratios of both nitrogen and carbon as a proxy for niche space. While the first three chapters investigate generalities in the patterns and drivers of diversification by comparing two independent radiations in the same “island-like” environment, Chapter fives takes a different approach by placing one of the Lake Tanganyika radiations, Synodontis, in its broader phylogenetic context. In this chapter morphological diversification is investigated in the largely riverine continental radiation of Synodontis found throughout sub-Saharan Africa. 3 Table of Contents Declaration ............................................................................................................................................. 2 Statement of authorship ................................................................................................................... 2 Abstract ................................................................................................................................................... 3 Table of Contents ................................................................................................................................. 4 Acknowledgements ........................................................................................................................... 14 Chapter 1 Lake Tanganyika and adaptive radiation 1.1 Adaptive Radiation - where are we now? ............................................................... 15 1.1.1 The study system ..................................................................................................... 17 1.2 Endemic Radiations of Lake Tanganyika ................................................................ 18 1.2.1 Cichlid fishes ............................................................................................................. 18 1.2.2 Non-cichlid radiations ........................................................................................... 20 1.2.3 Catfish (siluriforms) in Lake Tanganyika ....................................................... 21 1.2.4 Beyond Lake Tanganyika ..................................................................................... 23 1.3 Aims for the thesis ........................................................................................................... 24 1.4 References ........................................................................................................................... 26 Chapter 2 Nocturnal claroteine catfishes reveal dual colonisation but a single radiation in Lake Tanganyika 2.1 Abstract ................................................................................................................................ 34 2.2 Introduction ....................................................................................................................... 34 2.2.1 The study system ..................................................................................................... 36 2.3 Methods ............................................................................................................................... 37 2.3.1 Sampling ..................................................................................................................... 37 2.3.2 DNA extraction, amplification and sequencing............................................ 38 2.3.3 Phylogenetic inference .......................................................................................... 39 4 2.3.4 Molecular dating ...................................................................................................... 39 2.3.5 Species delimitation ............................................................................................... 41 2.4 Results .................................................................................................................................. 43 2.4.1 Model selection and phylogenetic analysis ................................................... 43 2.4.2 Estimation of molecular divergence dates .................................................... 44 2.4.3 Species delimitation ............................................................................................... 49 2.5 Discussion ........................................................................................................................... 50 2.5.1 Origins and colonisation history ....................................................................... 50 2.5.2 Diversification of the LT claroteine clade ...................................................... 50 2.5.3 Locally restricted diversity .................................................................................. 53 2.5.4 Taxonomy of LT claroteines ................................................................................ 54 2.5.5 Conclusions ................................................................................................................ 55 2.6 References ........................................................................................................................... 56 Chapter 3 Intralacustrine allopatry: differing geographic structure in two Lake Tanganyika catfish species 3.1 Abstract ................................................................................................................................ 61 3.2 Introduction ....................................................................................................................... 61 3.3 Methods ............................................................................................................................... 65 3.3.1 Sampling ....................................................................................................................
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