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Symbiodinium Diversity and Potential Hybridisation on the Highly Biodiverse Coral Reefs of Timor-Leste

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Symbiodinium Diversity and Potential Hybridisation on the Highly Biodiverse Coral Reefs of Timor-Leste Symbiodinium diversity and potential hybridisation on the highly biodiverse coral reefs of Timor-Leste Joshua Ian Brian A thesis submitted to the Victoria University of Wellington in partial fulfilment of the requirements for the degree of Master of Science in Marine Biology Victoria University of Wellington, New Zealand 2018 Atauro Island, Timor-Leste ii Abstract To persist in oligotrophic waters, reef-building corals rely on nutritional interactions with their intracellular symbionts: photosynthetic dinoflagellates of the genus Symbiodinium. This relationship is threatened by increasing environmental stress, which can stimulate loss of these symbionts from coral tissues (‘coral bleaching’). Members of the genus Symbiodinium display high levels of genetic diversity, and demonstrate a corresponding diversity in physiological responses to environmental change. However, the true diversity and potential for genetic adaptation in this genus remain poorly characterised. This thesis aimed to further the understanding of symbiont diversity and adaptive potential by conducting assessments of Symbiodinium at Atauro Island and the neighbouring Timor-Leste mainland. These sites have previously been shown to be of outstanding conservation value, with extremely high levels of coral diversity. Atauro Island also possibly hosts the highest diversity of reef fish in the world. However, the Symbiodinium communities at these sites have never been assessed. Two specific objectives were therefore addressed here. The first was to measure Symbiodinium diversity at Atauro Island (four sites) and Timor (three sites), using direct sequencing of three gene regions: cob gene, mitochondrion; ITS2 region, nucleus; and psbAncr region, chloroplast; in addition to Next Generation Sequencing of the ITS2 region. The second objective was to establish evidence for Symbiodinium hybridisation, a potentially rapid evolutionary mechanism that may facilitate adaptation to environmental stress, by looking for genetic incongruences between Symbiodinium organelles. Coral symbionts of Timor-Leste were found to be similar to those from other coral reefs of the Indo- Pacific, with several host generalist and multiple host specific types observed. However, there were also several novel Symbiodinium types found (C15p, C15q, C1x, C1z). Despite their geographic proximity, there were strong differences observed between the symbiont communities of Atauro Island and mainland Timor. In particular, the coral genus Pocillopora hosted clade C symbionts exclusively at Atauro Island, while it hosted clade D exclusively at Timor sites. Other symbiont types also showed geographic partitioning, and diversity was 1.25 times higher at Atauro Island, a figure consistent for the cob and ITS2 regions. While Timor sites have comparable Symbiodinium diversity to other reefs globally, Atauro has noticeably elevated Symbiodinium diversity. Next Generation Sequencing affirmed these patterns, with Atauro Island sites having much more diverse cryptic populations of Symbiodinium, largely driven by symbionts in clade C. The exception was clade D symbionts, which were proportionally far more diverse at Timor, a pattern consistent in multiple coral genera. There was strong evidence of genetic incongruence at two Atauro Island sites, with all testing procedures identifying genetic discordance between organellar and nuclear genomes, consistent with iii theoretical predictions of hybridisation. This study therefore presents strong evidence for Symbiodinium hybridisation, and its corroboration by multiple loci is significant. Putative hybrid Symbiodinium always had a common type as one of the possible parents, with a rarer symbiont as the other. For example, one putative hybrid had organellar genes of the common generalist Symbiodinium C40, while it was identified as the rare type C3z with the ITS2 region. Both of these Symbiodinium types were also found in congruent relationships, which strongly supports the possibility that they sexually reproduced to produce the incongruent putative hybrid. Environmental stressors, such as increased temperature, turbidity and sedimentation, are suggested reasons for lowered Symbiodinium diversity at Timor, as they may impose a selection pressure on corals to only keep highly beneficial symbionts. This reduction in diversity likely limits the potential for adaptive change through methods like hybridisation, and highlights the need to assess and conserve symbiont diversity to the same extent as coral diversity. iv Acknowledgements I would initially like to thank my two supervisors. Professor Simon Davy has provided a huge amount of support not just through this project but over the last four years, given me multiple opportunities to develop my skills and made himself available whenever required. Dr Shaun Wilkinson showed a large amount of ambition in helping to design the project as well as faith that I could carry it out, taught me so much about Symbiodinium genetics and how to be a modern adaptable scientist, and remained patient whenever I did weird things with the data. I am extremely grateful to them both. The scale of this project would not have been possible without multiple funding sources. I would like to acknowledge the William Georgetti Scholarship, the Alison Morton Scholarship, and the Victoria Graduate Award, in addition to a Rutherford Foundation Trust Postdoctoral Award to Shaun Wilkinson. I received assistance from many people during the fieldwork component of this research in Timor- Leste. Thanks are given to Shaun and Alice Wilkinson for generously hosting me in Dili (and particularly Alice for putting up with a DNA lab in the bathroom and coral samples in the freezer). Ricardo ‘Ricky’ Ximenes Marquez provided a huge amount of logistical assistance, and was made available through the generosity of Kevin Austin. Barry Hinton facilitated relationships with the local village. I am also grateful to the chief of the village of Beloi for granting us permission to sample in the Local Marine Managed Area. All biological samples in this thesis were collected with the permission of the government of Timor-Leste (Ministerio da Agricultura e Pescas, permit number LNC- PC0012.VI.16). I thank all past and present members of the Davy Lab. In particular, I acknowledge Dr Clint Oakley for his advice and making sure I had everything I needed, Grace Newson and Charlotte Völkel for speeding up the lab work at various points, as well as Dr Jennifer Matthews and Yasmin Gabay, for spending a large amount of time teaching me laboratory techniques and skills, and lending me reagents whenever my work exceeded my capacity to plan ahead. Everybody also showed remarkable tolerance to me having the radio on full blast for eight hours a day while doing my PCR clean-ups. To my surprise, many academics outside Victoria University were responsive to my unsolicited queries. I thank Dr David Swofford (Duke University) for confirming a bug in PAUP*, Dr Sarah Westcott (University of Michigan) for some tips on mothur, Dr Erik Franklin (Hawaii Institute of Marine Biology) for sending me the complete GeoSymbio database, in addition to Professor Arthur Grossman (Stanford University) and Dr John Parkinson (Oregon State University) who provided useful discussions on aspects of the thesis. v I am thankful to all those who made my Masters a happier time: Kate Irving, Roald Bomans, Jess Russell, Brianna Lawrence, Kayla Griffin, Bobby Lust, Lucy Gorman, Amir Mashini, Jordan Anderson and Schyana Sivanantham. You were more important than you realised. I would also like to direct my personal gratitude to the following: To Brittany Abels, Kennie Critchlow, and Hannah Brian – you kept me endlessly amused, and appeared to have an unwavering faith that I would get something decent in. To Grace Clendon – your formatting help was only the most meagre of your contributions to my past year. Finally, to my parents, Alan and Belinda – this thesis and indeed my university career would not have been possible without your unconditional love and support. You gave me the world – all I had to do was take it. vi Table of Contents Abstract …………………………………………………………………………………… iii Acknowledgements ……………………………………………………………………….. v Table of Contents …………………………………………………………………………. vii List of Figures …………………………………………………………………………….. x List of Tables ……………………………………………………………………………… xi Chapter 1: General Introduction ………………………………………………………... 1 1.1. Coral reefs and symbiosis ……………………………………………………… 1 1.1.1. Symbiosis ……………………………………………………………… 1 1.1.2. Symbiodinium and coral reefs …………………………………………. 2 1.1.3. Coral importance and threats ………………………………………….. 4 1.1.4. Coral bleaching ………………………………………………………... 5 1.2. Symbiont diversity ……………………………………………………………... 6 1.2.1. Recognition of diversity within Symbiodinium ………………………... 6 1.2.2. Summary of genetic tools used in Symbiodinium systematics ………… 8 1.2.3. Assessing diversity with the ITS2 ……………………………………... 10 1.2.4. Beyond the ITS2 ………………………………………………………. 13 1.3. Functional and ecological diversity of Symbiodinium …………………………. 14 1.3.1. Symbionts and temperature ……………………………………………. 14 1.3.2. Symbionts and other environmental factors …………………………... 15 1.3.3. Specific vs. general associations between corals and symbionts ……… 15 1.4. Mechanisms of adaptive change in the coral-algal symbiosis …………………. 17 1.4.1. ‘Switching’ and ‘shuffling’ ……………………………………………. 17 1.4.2. Host-symbiont co-adaptation ………………………………………….. 21 1.4.3. Symbiont sex and hybridisation ……………………………………….. 22 1.5. Aims and objectives
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