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Molecular Phylogeny and Seascape Genetics of the Panulirus Homarus Subspecies in the Western Indian Ocean

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Molecular Phylogeny and Seascape Genetics of the Panulirus Homarus Subspecies in the Western Indian Ocean Molecular phylogeny and seascape genetics of the Panulirus homarus subspecies in the Western Indian Ocean By Sohana Singh (MSc Genetics) Submitted in fulfilment of the academic requirements for the degree of Doctor of Philosophy in The School of Life Sciences University of KwaZulu-Natal Durban As the candidate’s supervisors we have approved this thesis/dissertation for submission. Signed: Name: Johan Groeneveld Date: 6 December 2017 Signed: Name: Sandi Willows-Munro Date: 5 December 2017 i Preface The work described in this dissertation was carried out at the Oceanographic Research Institute (ORI), which is affiliated with the School of Life Sciences at the University of KwaZulu-Natal, Westville. The study was undertaken between February 2015 and December 2017, under the supervision of Professor Johan Groeneveld and co-supervision of Dr Sandi Willows-Munro. It represents original work by the author and has not otherwise been submitted in any form for any degree or diploma to any tertiary institution. Where use has been made of the work of others it is duly acknowledge in the text. Sohana Singh Signed _________________ Date 7 December 2017 Prof. Johan Groeneveld Signed Date 6 December 2017 Dr. Sandi Willows-Munro Signed Date 5 December 2017 ii Declaration 1 - Plagiarism I, Sohana Singh, declare that: The research reported in this thesis, except where otherwise indicated, is my original research. This thesis has not been submitted for any degree or examination at any other university. This thesis does not contain other persons’ data, pictures, graphs or other information, unless specifically acknowledged as being sourced from other persons. This thesis does not contain other persons' writing, unless specifically acknowledged as being sourced from other researchers. Where other written sources have been quoted, then: Their words have been re-written but the general information attributed to them has been referenced. Where their exact words have been used, then their writing has been placed in italics and inside quotation marks, and referenced. This thesis does not contain text, graphics or tables copied and pasted from the Internet, unless specifically acknowledged, and the source being detailed in the thesis and in the references sections. Signed: Sohana Singh 7 December 2017 iii Declaration 2 – Publications Detail of contribution to publications that form part and/or include research presented in this thesis. Chapter 2 1. Singh SP, Groeneveld JC, Al-Marzouqi A, Willows-Munro S. (2017) A molecular phylogeny of the spiny lobster Panulirus homarus highlights a separately evolving lineage from the Southwest Indian Ocean. PeerJ 5:e3356 https://doi.org/10.7717/peerj.3356. 2. Singh SP, Groeneveld JC, Willows-Munro S. (2017) A molecular phylogeny of the spiny lobster Panulirus homarus highlights a separately evolving lineage from the Southwest Indian Ocean. Oral presentation at the Southern African Marine Science Symposium, July 2017, Port Elizabeth, South Africa. 3. Singh SP, Groeneveld JC, Willows-Munro S. (2017) A molecular phylogeny of the spiny lobster Panulirus homarus highlights a separately evolving lineage from the Southwest Indian Ocean. Oral presentation at the Western Indian Ocean Marine Science Symposium, October/November 2017, Dar-es-Salaam, Tanzania. Chapter 3 4. Singh SP, Groeneveld JC, Willows-Munro S. (2017) Comparative population genetics and phylogeography of the Panulirus homarus subspecies complex in the Southwest Indian Ocean. Oral presentation at the Southern African Marine Science Symposium, July 2017, Port Elizabeth, South Africa. iv Abstract The oceans are one of the world’s most dynamic environments. To cope with the constantly changing conditions brought about by climatic and physical forcing, its living inhabitants must adapt continually, or else they may not survive. This basic tenet of evolutionary change can explain the rich diversity of marine biota – a diversity which is also captured as genetic information at a molecular level. The present study represents a comprehensive genetic assessment of the spiny lobster Panulirus homarus from the Western Indian Ocean, relying on a multidisciplinary approach and different, though complementary lines of evidence. Phylogenetic-, phylogeographic- and population genetics analyses were performed, augmented with a seascape approach, to account for the influences of ocean currents, environmental variables and life history characteristics. Molecular markers appropriate for different timescales were chosen – to provide insights spanning from evolutionary epochs to fine-scale recent and contemporary events. In Chapter 2, a panel of mitochondrial and nuclear intron DNA markers were used in conjunction with fossil data, to examine the phylogenetic relationships between three Panulirus homarus subspecies. Concatenation of mitochondrial and nuclear markers strongly supported the status of P. h. rubellus (the red southern form from the Southwestern Indian Ocean) as a distinct species. Divergence dating analysis estimated that P. h. rubellus and the other two subspecies (P. h. homarus from the Indo-West Pacific and P. h. megasculptus from the Arabian Sea combined) diverged from a common ancestor approximately 26 million years ago (MYA), during the Oligocene. P. h. rubellus is estimated to have arisen between 10 and 16 MYA during the Miocene, possibly in response to the final closure of the Tethys Sea and associated changes in global ocean circulation patterns. An analysis of demographic history in Chapter 3 indicated that P. homarus underwent a population decline and subsequent expansion during the Pleistocene, when sea-level rise, warming and strengthened ocean currents after the last glacial maxima would have promoted a southerly expansion of P. h. rubellus. Faster-evolving microsatellite data revealed incipient genetic structure between P. h. homarus and P. h. megasculptus, which could not be observed from the more conserved mitochondrial loci. This suggests that larvae of P. h. megasculptus are retained in the contemporary Arabian Sea circulation, influenced by the seasonally reversing Somali Current and eddies off Oman and Somalia. v Empirical genetic data were correlated with ocean circulation based on a particle simulation model of larval dispersal, using a CBOCM in Chapter 4. Particle simulations over a 120 day period broadly supported the patterns observed in the genetic data. Spatially explicit genetic clustering methods using the microsatellite data identified a genetic discontinuity/ transition zone near Zavora in south-central Mozambique, with P. h. homarus occurring to the north and P. h. rubellus to the south. Migration analysis using information from all markers in Chapter 3 showed that gene flow across the Mozambique Channel, from Madagascar to the African shelf, occurs from east to west, and that the population in southeast Madagascar is self-recruiting. The results are congruent with the ‘suitcase hypothesis’, that larvae become entrained in eddies where the East Madagascar Curent rounds southern Madagascar, and are then transported across the Mozambique Channel towards the African mainland shelf. Both the genetic data and CBOCM larval dispersal simulations supported this pattern. The CBOCM suggests that P. h. rubellus larvae that stray off the mainland continental shelf and into the Agulhas Current will rapidly be displaced southwestwards, beyond the range of benthic P. homarus populations. These larvae will most likely be lost. The narrow continental shelf off eastern South Africa may therefore form a bottleneck for dispersing larvae. The Seascape analyses of effects of environmental variables on genetic differentiation suggested that sea surface temperature along a latitudinal gradient can partially explain the diversification into the subtropical P. h. rubellus lineage and the more tropical P. h. homarus lineage. The recurrent patterns emerging from all lines of evidence in this study (genetic, oceanography and environment) are that climatic fluctuations, which affect ocean currents and other oceanic variables, are in turn responsible for genetic connectivity or diversity in P. homarus. These observations can facilitate more informed predictions on how changing climates may impact the diversity of marine life. vi Acknowledgements This thesis is dedicated to the memory of my late grandfather, who always wanted me to become a doctor. I would like to thank the NRF (Professional Development Programme) for the funding granted to my supervisor, which was used to fund my living expenses and to ORI and SAAMBR for providing office and IT infrastructure for the duration of this project. I would like to express my sincere gratitude to my supervisor Prof. Johan Groeneveld for the continuous support of my Ph.D study, for his patience, motivation, inspiration and immense knowledge and speedy feedback on my writing of the chapters. His guidance helped me throughout the research and writing of this thesis. Thank you to my co-supervisor, Dr Sandi Willows-Munro, who has contributed a great deal towards my growth as a scientist by providing me with so many of the opportunities that I received. Thank you for your invaluable advice and comments on this work. A big thank you to Desmond Hayes, Jade Maggs, Stuart Dunlop, Jenna Keightley, Maggie Reddy, Elizabeth Mueni (Kenya), Lourenzo Zacarias (Mozambique), Abdulaziz Al- Marzouqi (Oman & Yemen), Suitcase Project (Madagascar), who were involved in collection of lobsters for this study. Additionally, thank you to Simon
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