THE CONSERVATION and LANDSCAPE GENETICS of the SAND LIZARD Lacerta Agilis

A University of Sussex DPhil thesis Available online via Sussex Research Online: http://sro.sussex.ac.uk/ This thesis is protected by copyright which belongs to the author. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the Author The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the Author When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given Please visit Sussex Research Online for more information and further details THE CONSERVATION AND LANDSCAPE GENETICS OF THE SAND LIZARD Lacerta agilis Liam Russell Thesis submitted for the Degree of Doctor of Philosophy School of Life Sciences University of Sussex December 2012 …this ‘aristocrat’ needs our special care, a quiet large castle to live in and plenty of time to grow old. Only then can we preserve it for our children. H. Strijbosch, Nijmegen, 1988 Summary UNIVERSITY OF SUSSEX Liam Russell Doctor of Philosophy The Conservation and Landscape Genetics of the Sand Lizard Lacerta agilis SUMMARY Lacerta agilis is a widespread lizard which reaches the western edge of its range in Britain where it is restricted to three geographically separated areas. Recent habitat loss and fragmentation have resulted in a significant decline and it is now a UK conservation priority. Sand lizards from across the Britain were genotyped at 15 microsatellite loci and the resulting dataset used to address questions regarding the conservation genetics, phylogeography and influence of landscape on patterns of genetic diversity. Genetic diversity of Dorset populations compared favourably to European examples. However, diversity was significantly lower in Surrey and Merseyside. Significant genetic structuring occurred across small geographical distances even in relatively unfragmented landscapes. Lacerta agilis colonised Britain via a land bridge across the North Sea and reached the limits of its current distribution approximately 5,000 years BP. Subsequent climate cooling has resulted in a range contraction to areas where the habitat is suitable for the successful incubation of eggs. A resistance surface was used to investigate the effect of landscape configuration on patterns of genetic diversity at multiple scales in Dorset. At a local scale, habitat type and rivers were the best predictors of genetic diversity. At a regional scale, rivers were most important, whereas habitat type and artificial barriers were less important. Artificial barriers may be more significant than the results suggest as their true effect has not yet been realised due to a genetic time-lag. Male lizards from Merseyside exhibited significant differences in colour and pattern to the Dorset and Surrey populations. However, despite difference in colour, all populations were equally green, which is in keeping with the importance of ‘greenness’ as a sexual signal. The implications of these findings for the conservation of L. agilis are discussed in the context of current challenges and predicted future global climate change. iii Contents CONTENTS SUMMARY ......................................................................................................................... iii CONTENTS ......................................................................................................................... iv LIST OF FIGURES ................................................................................................................. vi LIST OF TABLES ................................................................................................................. viii DECLARATION ..................................................................................................................... x ACKNOWLEDGEMENTS ....................................................................................................... xi 1 INTRODUCTION ........................................................................................................... 1 1.1 Introduction .................................................................................................................. 1 1.2 Habitat Loss and Fragmentation ................................................................................... 1 1.3 Landscape Genetics....................................................................................................... 7 1.4 Loss and Fragmentation of Lowland Heathland ......................................................... 14 1.5 Sand Lizards................................................................................................................. 17 1.6 Aims of this Thesis....................................................................................................... 26 2 GENERAL MATERIALS AND METHODS ......................................................................... 29 2.1 Introduction ................................................................................................................ 29 2.2 Sampling Strategy ....................................................................................................... 29 2.3 Sample Sites ................................................................................................................ 32 2.4 Field Sampling ............................................................................................................. 35 2.5 Genotyping .................................................................................................................. 36 2.6 Analysis of Microsatellite Data ................................................................................... 38 3 CONSERVATION GENETICS AND PHYLOGEOGRAPHY OF BRITISH SAND LIZARDS .......... 42 3.1 Introduction ................................................................................................................ 42 3.2 Materials and Methods ............................................................................................... 43 3.3 Results ......................................................................................................................... 46 3.4 Discussion .................................................................................................................... 68 4 LANDSCAPE GENETICS OF SAND LIZARDS IN DORSET .................................................. 77 4.1 Introduction ................................................................................................................ 77 4.2 Materials and Methods ............................................................................................... 80 4.3 Results ......................................................................................................................... 90 4.4 Discussion .................................................................................................................. 101 5 GEOGRAPHIC VARIATION OF COLOUR AND PATTERN IN BRITISH SAND LIZARDS ....... 111 5.1 Introduction .............................................................................................................. 111 iv Contents 5.2 Materials and Methods ............................................................................................. 115 5.3 Results ....................................................................................................................... 118 5.4 Discussion .................................................................................................................. 125 6 GENERAL DISCUSSION .............................................................................................. 128 6.1 Introduction .............................................................................................................. 128 6.2 Summary of Thesis Aims and Results........................................................................ 128 6.3 Current Challenges for the Conservation of Lacerta agilis ....................................... 130 6.4 Potential Effects of Climate Change.......................................................................... 132 6.5 Opportunities for Further Research .......................................................................... 134 6.6 Conclusion ................................................................................................................. 135 REFERENCES .................................................................................................................... 136 APPENDIX 1: PAIRWISE DPS VALUES BETWEEN DORSET SITES .............................................. A1 APPENDIX 2: PARAMETERISATION OF HIGH RESISTANCE FEATURES ................................... A2 APPENDIX 3: G’ST, D AND DPS MULTIPLE REGRESSION MODELS ............................................ A4 v List of Figures LIST OF FIGURES The ‘aristocrat’. Male sand lizard from Wareham Forest, Dorset ................................................. ii From G.A. Boulenger (1916): On the Lizards allied to Lacerta muralis, with an Account of Lacerta agilis and L. parva. Plate I. Lacerta agilis. ....................................................................... xiii Figure 1.1. Relationship between geographic distance (X axis) and genetic distance (Y axis) in the eastern collared lizard Crotaphytus collaris in different landscape configurations.. ............. 8 Figure 1.2. Example of Least Cost Path (LCP) on a hypothetical resistance surface................... 10 Figure 1.3.

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