Population genetics and sociality in the Sungazer (Smaug giganteus)

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 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