PATTERNS AND PROCESSES OF ADAPTATION IN LACERTID LIZARDS TO ENVIRONMENTS IN SOUTHERN AFRICA Shelley Edwards Dissertation presented for the degree of Doctor of Philosophy (Zoology) in the Faculty of Science at Stellenbosch University Supervisor: Dr Krystal Tolley (SANBI; Stellenbosch University)*$ Co-supervisor: Prof Le Fras Mouton (Stellenbosch University)$ * Applied Biodiversity Research, South African National Biodiversity Institute, Rhodes Drive, Newlands, South Africa 7735. $ Department of Botany and Zoology, University of Stellenbosch, Private Bag X1, Matieland, South Africa 7602 DECEMBER 2013 Stellenbosch University http://scholar.sun.ac.za Stellenbosch University http://scholar.sun.ac.za CONTENTS DECLARATION II ABSTRACT III OPSOMMING IV ACKNOWLEDGEMENTS V LIST OF FIGURES VI LIST OF TABLES VIII GENERAL INTRODUCTION 2 Species variation 3 Cryptic species 4 Phenotypic plasticity 5 Rapid morphological diversification 5 Adaptive radiations vs. non-adaptive radiations 6 Background to lacertid lizards 6 Systematic relationships within the family Lacertidae 7 Motivation 9 AIMS AND OBJECTIVES 11 1. CONVERGENT MORPHOLOGIES ASSOCIATED WITH HABITAT STRUCTURE HAVE LED TO THE MISCLASSIFICATION OF SPECIES 12 Introduction 13 Materials and Methods 14 Sampling 14 Laboratory protocols 14 Genetic analyses 15 Characterization of habitat type 16 Morphometric analyses 18 Results 20 Discussion 24 Conclusions 27 2. DIETARY PREFERENCE DETERMINES CRANIAL SHAPE WITHIN THE SANDVELD LIZARDS NUCRAS 28 Introduction 29 Materials and Methods 31 DNA extraction and sequencing 31 Phylogenetic tree estimations 31 Linear morphometric analyses 32 Dietary analyses 32 Geometric morphometric analyses 33 Performance analyses 36 Statistical analyses 36 Phylogenetic comparative analyses 37 Results 37 Phylogenetic relationships and morphological clustering of all Nucras 37 Dietary, morphological and performance analyses of five Nucras species 41 Phylogenetic comparative analyses 44 Discussion 45 Conclusions 47 i | P a g e Stellenbosch University http://scholar.sun.ac.za 3. THE ADAPTIVE NATURE OF THE RADIATIONS WITHIN THE GENUS MEROLES AND THE RESULTANT EFFECTS ON PERFORMANCE 48 Introduction 49 Materials and Methods 51 Sampling 51 Geometric morphometric analyses 52 Performance analyses 53 Phylogenetic comparative methods 53 Results 54 Morphometric and performance analyses 54 Phylogenetic comparative analyses 59 Discussion 62 Conclusion 64 4. DISPARITIES BETWEEN MORPHOLOGY AND PHYLOGENY IN A WIDE-RANGING LACERTID SPECIES PEDIOPLANIS LINEOOCELLATA. 65 Introduction 66 Materials and Methods 67 DNA extraction and sequencing 67 Phylogenetic analyses 69 Morphometric analyses 70 Results 70 Phylogenetic analyses 70 Morphological analyses 73 Discussion 76 Conclusions 78 5. RAPID EVOLUTION OF MORPHOLOGY AND PERFORMANCE AFTER AN INTRODUCTION INTO A NOVEL HABITAT IN KNOX'S OCELLATED SAND LIZARD MEROLES KNOXII. 80 Introduction 81 Materials and Methods 84 Sampling 84 Genomic DNA extraction, amplification and sequencing 84 Population genetics analyses 84 Linear morphometric analyses 85 Performance analyses 86 Habitat assessments 86 Results 87 Population genetic structure 87 Linear morphometric analyses 87 Performance analyses 91 Habitat analyses 91 Discussion 94 Conclusions 95 CONCLUSIONS AND SUMMARY OF DISSERTATION 96 Taxonomic considerations 98 Last thoughts… 99 REFERENCES 101 APPENDIX A: SUPPLEMENTARY INFORMATION 110 APPENDIX B: PAPERS PUBLISHED, IN PRESS OR IN PREPARATION 130 List of published papers attached in Appendix B: 130 List of manuscripts in preparation: 130 ii | P a g e Stellenbosch University http://scholar.sun.ac.za DECLARATION By submitting this dissertation electronically, I declare that the entirety of the work contained therein is my own original work, that I am the sole author thereof (save to the extent explicitly otherwise stated), that reproduction and publication thereof by Stellenbosch University will not infringe any third party rights and that I have not previously in its entirety or in part submitted it for obtaining any qualification. 26-08-2013 Cape Town …………………………. …………………………. …………………………… Signature Date Location Copyright © 2013 Stellenbosch University All rights reserved ii | P a g e Stellenbosch University http://scholar.sun.ac.za ABSTRACT The phenotype of an individual has often been used as the descriminating factor in distinguishing species. However, with the advent of more precise molecular techniques, the genotype of species is increasingly being used as the preferred method in taxonomic classifications. Many taxa have recently been demonstrated to be incongruent in terms of their genetic and morphological groupings, and this may due to the influence that the environment may have on the morphological and functional aspects of a species. Selective pressures often act upon the performance of a species within a particular habitat first, and then selection for the morphological characters that allow for optimal performance occurs. Should genetically disparate species inhabit a particular environment, convergence in morphologies and performance may evolve. Historically, lizard species descriptions were based primarily on external morphologies, and thus misclassfication of species may have occurred due to mistakenly grouping species with convergent morphologies together. In the current dissertation, the links between morphology, performance capacities, diet and behaviour is explored in comparison to the environment and genetic relationships of southern African lacertid lizards. The performance capacities and associated morphological traits were expected to be more closely linked with the environment, and not closely linked with genetic relationships. To investigate these expectations, a multidisciplinary approach was taken, and genetic, morphological and performance analyses were done and compared with dietary behavioural and environmental analyses. In the first chapter, the link between habitat openness and the lizard bauplans is investigated and the presence of convergent morphologies within this group of lizards is uncovered. These convergences are shown to have resulted in misclassification of two lacertid species, and taxonomic revisions within the family are discussed. The second chapter explores the link between performance and associated morphological traits, and the dietary composition of the members of the Nucras genus. The third chapter identifies the link between the predator escape strategies employed by the members of the Meroles genus, and their morphologies and performance capacities. The fourth chapter explores the intraspecific, inter-population differences in morphologies and investigates the link between the morphological groupings and the population genetic groupings within Pedioplanis lineoocellata. The final chapter identifies whether adaptation to a novel habitat can occur over a relatively short period of time, and the morphological traits, functional aspects, and population genetic structure is investigated in conjunction with environmental analyses of vegetation and substrate between the populations of Meroles knoxii. It was concluded that the morphological and functional aspects of the southern African lacertid lizards are more closely related to the environment, particularly the microhabitat structure, than to their genetic relationships, and that future work using this group of lizards should involve a multidisplinary approach as different selective pressures are playing a role in shaping the morphologies and performance capacities of these lizards, compared to those that are acting upon the genotypes of the lizards. iii | P a g e Stellenbosch University http://scholar.sun.ac.za OPSOMMING Die fenotipe van 'n individu is dikwels gebruik as die diskriminerende faktor in kenmerkende spesies. Maar, met die ontwikkeling van meer akkurate molekulêre tegnieke, word die genotipe van spesies toenemend gebruik as die voorkeur-metode in taksonomiese klassifikasie. Die onversoenbaarheid van genetiese en morfologiese eienskappe kom voor in ‘n verskeidenheid taksa, dit kan wees as gevolg van die invloed wat die omgewing het op die morfologiese en funksionele aspekte van ‘n spesie. Selektiewe druk beїnvloed dikwels doeltreffende funktionaliteit van 'n spesie in 'n bepaalde habitat eerste, en gevolglik word morfologiese karakters wat voorsiening maak vir optimale funktionaliteit geselekteer. Indien geneties uiteenlopende spesies woon in 'n bepaalde omgewing, kan konvergensie in morfologie en soortgelyke werksverrigtinge ontwikkel. Histories, is akkedis spesiesbeskrywings hoofsaaklik gebaseer op eksterne morfologieë, en kan dus misklassifikasie tot gevolg hê wat kan lei tot foutiewe taksonomie van spesies met konvergente morfologieë. In die huidige verhandeling, is die verband tussen die morfologie, werksverrigtingsvermoë, dieët en gedrag ondersoek, in vergelyking met die omgewing en die genetiese verwantskappe van Suider-Afrikaanse sandakkedisse. Die werksverrigtingsvermoë en gepaardgaande morfologiese eienskappe word verwag om te meer verband te hou met die omgewing, en dus nie in noue verband te wees met die genetiese verwantskappe nie. Om hierdie verwagtinge te ondersoek, is 'n multi-dissiplinêre benadering geneem, en genetiese, morfologiese en werksverrigting- ontledings is gedoen in vergelyking met dieët, gedrags-en omgewings-ontleding. In die eerste hoofstuk, is die skakel tussen die habitat openheid en die akkedis bauplans ondersoek en die teenwoordigheid van konvergente morfologieë binne hierdie groep akkedisse word ten