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The Sclerotic Ring: Evolutionary Trends in Squamates

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The Sclerotic Ring: Evolutionary Trends in Squamates The sclerotic ring: Evolutionary trends in squamates by Jade Atkins A Thesis Submitted to Saint Mary’s University, Halifax, Nova Scotia in Partial Fulfillment of the Requirements for the Degree of Master of Science in Applied Science July, 2014, Halifax Nova Scotia © Jade Atkins, 2014 Approved: Dr. Tamara Franz-Odendaal Supervisor Approved: Dr. Matthew Vickaryous External Examiner Approved: Dr. Tim Fedak Supervisory Committee Member Approved: Dr. Ron Russell Supervisory Committee Member Submitted: July 30, 2014 Dedication This thesis is dedicated to my family, friends, and mentors who helped me get to where I am today. Thank you. ! ii Table of Contents Title page ........................................................................................................................ i Dedication ...................................................................................................................... ii List of figures ................................................................................................................. v List of tables ................................................................................................................ vii Abstract .......................................................................................................................... x List of abbreviations and definitions ............................................................................ xi Acknowledgements ..................................................................................................... xii 1.0 Introduction ............................................................................................................. 1 1.1 The vertebrate ocular skeleton ............................................................................. 1 1.2 The reptilian ocular skeleton ................................................................................ 2 1.3 Skeletal morphology: Influenced by environment and/or behaviour .................. 4 1.3.1 The ocular skeleton: Influenced by environment and/or behaviour ............. 5 1.4 Ocular skeletal development in reptiles ............................................................... 7 1.5 Squamata: A diverse order of reptiles .................................................................. 8 1.6 Limbless squamates pose a problem for phylogenetic analyses ........................ 10 1.6.1 Serpentes ..................................................................................................... 10 1.6.2 Amphisbaenia ............................................................................................. 11 1.6.3 Dibamids ..................................................................................................... 12 1.7 Using the ocular skeleton to resolve the squamate phylogeny .......................... 13 1.8 Objectives .......................................................................................................... 14 2.0 Methods ................................................................................................................. 15 2.1 Investigating sclerotic ring presence/absence in extinct and extant squamates . 15 2.1.1 Extant specimen database ........................................................................... 15 2.1.2. Fossil specimen database ........................................................................... 17 2.2 Phylogenetic mapping of the sclerotic ring ....................................................... 18 2.3 Life history and behaviour of squamates ........................................................... 20 3.0 Results ................................................................................................................... 23 3.1 Overview of the presence and absence of the sclerotic ring in squamates ........ 23 3.2 Phylogenetic mapping of the sclerotic ring character trait ................................ 25 3.2.1. Gauthier et al. (2012) morphological phylogeny using fossil data ............ 26 3.2.2 Gauthier et al. (2012) morphological phylogenies using extant data ......... 27 3.2.3 Kearney et al. (2003) morphological phylogeny using extant and fossil data ........................................................................................................................................ 29 3.2.4 Pyron et al. (2013) molecular phylogeny using extant data ....................... 31 3.3 Environment, behaviour, and limb morphology of extant squamates ............... 33 3.3.1 Squamate behaviour .................................................................................... 33 3.3.2 Sclerotic ring measurements ....................................................................... 37 4.0 Discussion .............................................................................................................. 44 4.1 On the fossil specimens and the loss of the sclerotic ring in evolutionary history ........................................................................................................................................ 45 iii 4.2 One loss and one secondary gain of the sclerotic ring in Squamata lineages is supported by morphological phylogenetic evidence ...................................................... 47 4.2.1 One loss of the sclerotic ring occurred within Amphisbaenia .................... 48 4.2.2 One loss and one secondary gain of the sclerotic ring occurred in Squamata ........................................................................................................................................ 50 4.3 Three individual losses of the sclerotic ring in Squamata lineages is supported by molecular phylogenetic evidence .............................................................................. 52 4.4 Comparison of the Gauthier et al. (2012) and Pyron et al. (2013) phylogenies with the Conrad (2008) phylogeny ................................................................................ 53 4.5 Together, developmental and evolutionary evidence supports three individual sclerotic ring losses ........................................................................................................ 55 4.5.1 Developmental evidence ............................................................................. 55 4.5.2 Evolutionary evidence ................................................................................ 56 4.6 The squamate species that lack a sclerotic ring are united by their headfirst burrowing ancestry, reduced limbs, and other shared traits ........................................... 58 4.6.1 Morphological variation between limbless lineages may account for the loss of the sclerotic ring ................................................................................................. 60 4.6.2. A scotopic past? ......................................................................................... 61 4.6.3 Rhineuridae is an example of extreme habitat and speciation events ......... 62 4.7 The morphology of the sclerotic ring is a good indicator of environment and behaviour ........................................................................................................................ 63 5.0 Summary and conclusions ..................................................................................... 65 6.0 Literature cited ....................................................................................................... 67 Appendix A1: Extant specimens assessed for this project .......................................... 78 Appendix A2: Extant specimens assessed for this project .......................................... 81 Appendix A3: Fossil specimens assessed for this project ........................................... 96 Appendix B: Raw data for sclerotic ring measurements ........................................... 109 Appendix C: Statistical analyses ............................................................................... 114 iv List of figures Figure 1.1 The ocular skeletal morphology in reptiles. 3 Figure 1.2 The two current phylogenies for Squamata. 10 Figure 2.1 Schematic of a sclerotic ring showing the measurements 21 used for analyses. Figure 3.1 Family level phylogeny of extant squamates modified 24 from Gauthier et al. (2012). Figure 3.2 Family and higher-level phylogeny showing 25 presence/absence of a sclerotic ring in fossil taxa modified from Gauthier et al. (2012), and Mo et al. (2010). Figure 3.3 Maximum parsimony (strict consensus) phylogeny of 28 more derived squamate relationships, modified from Gauthier et al. (2012). Figure 3.4 Bayesian phylogeny of more derived squamate 29 relationships, modified from Gauthier et al. (2012). Figure 3.5 Phylogeny of extant and fossil amphisbaenian 30 relationships, modified from Kearney (2003). Figure 3.6 Family and higher-level molecular phylogeny modified 32 from Pyron et al. (2013). Figure 3.7 Phylogeny modified from Gauthier et al. (2012) showing 34 families where scotopic species (black lines) and photopic species (green lines) are present. Figure 3.8 Phylogeny modified from Gauthier et al. (2012) showing 35 families where a fossorial lifestyle has evolved in some or all species. Figure 3.9 Phylogeny modified from Gauthier et al. (2012) showing 36 families where reduced limbs or complete limblessness has evolved in some or all species. Figure 3.10 Phylogeny modified from Gauthier et al. (2012) showing 37 the families where inner and outer sclerotic ring diameters were measured. v Figure 3.11 Scatterplot showing the
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