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Population Genetics and Sociality in the Sungazer (Smaug Giganteus)

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Population Genetics and Sociality in the Sungazer (Smaug Giganteus) Population genetics and sociality in the Sungazer (Smaug giganteus) Shivan Parusnath Doctoral Thesis Supervisors: Prof. Graham Alexander Prof. Krystal Tolley Prof. Desire Dalton Prof. Antoinette Kotze A thesis submitted to the Faculty of Science, University of the Witwatersrand, Johannesburg, in fulfilment of the requirements for the degree of Doctor of Philosophy. 30th October 2020 “My philosophy is basically this, and this is something that I live by, and I always have, and I always will: Don't ever, for any reason, do anything, to anyone, for any reason, ever, no matter what, no matter where, or who, or who you are with, or where you are going, or where you've been, ever, for any reason whatsoever.” - Michael G. Scott DECLARATION I declare that this thesis is my own, unaided work. It is being submitted for the Degree of Doctor of Philosophy at the University of the Witwatersrand, Johannesburg. It has not been submitted before for any degree or examination at any other University. All protocols were approved by the University of the Witwatersrand Animal Ethics Screening Committee (2014/56/B; 2016/06/30/B), and the National Zoological Garden, South African National Biodiversity Institute (NZG SANBI) Research, Ethics and Scientific Committee (P14/18). Permits to work with Threatened or Protected Species were granted by the South African Department of Environmental Affairs (TOPS59). Permits to collect samples in the Free State and Mpumalanga provinces were provided by Department of Small Business Development, Tourism and Environmental Affairs (01/34741; JM938/2017) and Mpumalanga Tourism and Parks Agency (MPB. 5519) respectively. Research approval in terms of Section 20 of the Animal Diseases Act (35 of 1984) was granted by the South African Department of Agriculture, Forestry and Fisheries (12/11/1/1/18). All samples used in this project were stored at the National Zoological Garden Biobank in Pretoria. Shivan Parusnath 30th Day of October 2020 i ABSTRACT Establishing links between the evolution and ecology of a species is one of the central facets of organismal biology. Quantifying the past and present flow of genetic material between populations can provide insight into the landscape features and associated environmental variables that impede or facilitate this process. An integrative approach utilising a) genetic markers that evolve at different evolutionary rates, b) ecological niche models that indicate niche suitability across a landscape, and c) knowledge of the life-history, social system, and morphology of a species can allow for the formulation and testing of hypotheses of scenarios of genetic structure in a species. The Sungazer (Smaug giganteus) is a large cordylid lizard endemic to the Highveld grasslands of South Africa. It is unique amongst the Cordylidae family because of its adherence to primary grassland, reliance on self-excavated burrows as long-term refuge sites, and organisation of multiple Sungazer burrow systems into spatially discrete colonies. Young Sungazers are often seen sharing burrows with adults, and because of this behaviour and the unique spatial organisation of colonies, the species has long been touted as potentially exhibiting kin-based sociality. Little is known about the dispersal ability of Sungazers, the levels of genetic differentiation within and between colonies, the processes that influence genetic structure in the species, and the existence of kin-based sociality in the species. The primary aim of this thesis was to investigate the population and social structure of S. giganteus at multiple spatial and evolutionary scales, using mitochondrial DNA, nuclear DNA, and species-specific microsatellites. Smaug giganteus occurs in five distinct genetic populations across its distribution (Western 1, Western 2, Central, Eastern 1, Eastern 2), that belong to three divergent phylogenetic clades (Western, Central, Eastern). The genetic differentiation of these clades correlate spatially and temporally with geological features that arose during the most recent uplift of the eastern Great Escarpment, ~900 m into the Highveld grasslands, ~2.5-1.8 MYA. Within these clades, a combination of barriers such as mountains, rivers, and isolation by distance appear to be the primary drivers of population structure. The average Sungazer body size (snout-vent-length and mass) in each clade was significantly different, with an increasing size gradient from west to east. This size gradient correlates with an increase in elevation and precipitation, and decrease in temperature, and may result from local adaption to different climatic niches in these vicariant populations. Sungazer colonies comprise primarily of extended family members, and Sungazers are significantly more related to individuals within the same colony than to those in other colonies. Sungazers that share burrows tend to be immediate family members. Juveniles, in most cases, occupied burrows with either their mother or father, and full-siblings. The behaviours of refuge sharing by adults and their ii offspring, combined with delayed juvenile dispersal, are indicative of parental care in the species. Besides the sharing of burrows with nuclear family members, social structure within colonies appears to be relatively homogenous, likely due to the frequent moves between burrows by adults during mating periods. This is the first evidence of kin-based sociality in an African lizard. The new insights into genetic structure in S. giganteus presented in this thesis have ramifications for how long-term conservation and translocation strategies for S. giganteus are managed, such that the genetic structure and health of populations are preserved. This study extends the evidence of lizard family living to a new taxonomic group, and a new continent, elucidating the reality that kin-based sociality may be more widespread in lizards than has long been thought. This opens the door to studies of kin-based sociality in other cordylids and African lizards, as well as more detailed research on the complex system of sociality in S. giganteus. iii ACKNOWLEDGMENTS The research presented in this thesis would have not been possible without the assistance, cooperation and friendliness of many, many landowners across the distribution of the Sungazer. The respect and interest that these individuals maintain for Sungazers gives me a lot of hope that the species is in good hands. Some of my finest memories from the past decade have been driving their dirt roads and walking their open fields in search of Sungazers. This project came with considerable financial costs of fieldwork, labwork, and keeping me alive. Project funding provided by the National Zoological Gardens (previously under NRF, now under SANBI), the Rufford Foundation (Second Grant: 13956-2), the National Geographic Society (Young Explorer Grant: C288-14), and the Alexander Herp Lab, allowed for the collections of hundreds of samples from the field, developing and testing microsatellite markers, and processing these samples in the lab. Funding through the NRF Professional Development Plan allowed for me to pay for rent and food, and live a comfortable life for the first three years of my PhD. It became a hustle after that, but my parents, Vinesh and Sashi Parusnath (and my third parent, Prianka), were always there to help pay bills when times got tough. I cannot be appreciative enough of their support, long after the normal duties of parenthood had passed. I owe an immeasurable thank you to the Carnegie Corporation of New York for a grant awarded to University of the Witwatersrand for the Next Generation of African Scholars, which covered in full, my final year of PhD fees. To complete this PhD without fee debt is truly a rare gift. Thank you. My supervisors, Graham Alexander, Krystal Tolley, Desire Dalton, and Antoinette Kotze were vital mentors to me on my journey of genetics, ecology and evolution. Each of you has imparted valuable life lessons onto me in multifarious ways. In particular I would like to thank Krystal Tolley and Graham Alexander who make for a supervisory dream team. Any student to have either of you supervising them can consider themselves lucky, but to land the pair is indeed great fortune. I think it was Tolkien that said, “in the company of friends, peril becomes adventure”. Wade Stanton- Jones, Thilo Beck, Mareike Dinberger, Hiral Naik, Bevan Dell, Ashadee Miller, and Mimmie Kgaditse all assisted in collecting tissue samples and making difficult decisions in the field. Thanks for the adventures. Wade in particular, who also spent several years doing research on Sungazers, was always a welcome field companion. Not only for the assistance, but for the great conversations about Sungazers, and the many memories made in the field together. Special thanks must also be given to Allan Vorster, who has welcomed me to Welkom on many occasions, to show friends, colleagues and film crews the colony of Sungazers that he watches over. He has also shared many interesting observations and photographs of Sungazers with me that have stimulated enthralling discussion. iv While labwork may appear to be more comfortable and simple than fieldwork to the uninitiated, this could not be further from the truth. It can in fact be far more terrifying. Many skilled students and technicians at the National Zoological Gardens taught me the ropes, and were always available to help solve problems. Almero Oosthuizen, Thabang Madisha, Antonie Kloppers, and Clearance Mnisi in particular made labwork more accessible. My labmates at the Alexander Herp Lab at Wits provided support in various ways throughout the PhD. In particular, Dr. Hanlie Engelbrecht went far beyond her duties as a post-doc in assisting me with the complex statistical analyses involved in this study. Her fervour to teach and upskill others is something that I endeavour to match. I hope to in turn pass these lessons and skills on to others. Other staff members at Wits have also served as important mentors to me, Stuart Sym, Dave Mycock, Marcus Byrne, and Carol Still chief among them. A special thanks also to Rose Sephton-Poultney, who proofread my thesis before submission.
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