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Taxonomy, Ecology and Conservation Genomics of North-Eastern Australian Earless Dragons (Agamidae: Tympanocryptis Spp.)

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Taxonomy, Ecology and Conservation Genomics of North-Eastern Australian Earless Dragons (Agamidae: Tympanocryptis Spp.) TAXONOMY, ECOLOGY AND CONSERVATION GENOMICS OF NORTH-EASTERN AUSTRALIAN EARLESS DRAGONS (AGAMIDAE: TYMPANOCRYPTIS SPP.) KIRILEE JANE CHAPLIN Bachelor of Science (Hons) Submitted in total fulfilment of the requirements of the degree of DOCTOR OF PHILOSOPHY JUNE 2018 School of BioSciences The University of Melbourne Taxonomy, Ecology and Conservation Genomics of North-Eastern Australian Earless Dragons (Agamidae: Tympanocryptis spp.) By Kirilee Chaplin © 2018 Supervisors: Jane Melville and Joanna Sumner Title Page: Tympanocryptis darlingensis sp. nov., photo by K. Chaplin ABSTRACT Land clearing and modification of natural habitats is threatening biodiversity globally. In Australia, most native grassland habitats have been heavily modified for agriculture, including cropping and grazing. Grassland specialist species, including earless dragon lizards (Tympanocryptis spp.) in north-eastern Australia, are of conservation concern due to this continued habitat loss and fragmentation. However, the north-eastern Australian group of earless dragons (including the recently described T. condaminensis, T. wilsoni and T. pentalineata) are at significant risk, due to the presence of multiple undescribed cryptic Tympanocryptis lineages within this region. It is imperative that the taxonomy is resolved for these cryptic lineages of conservation concern, so conservation of these species may occur. One of the major challenges for taxonomists in recent times has been the species delimitation of morphologically cryptic taxa. The detection of distinct molecular lineages within cryptic genera has increased exponentially over the past decades with advances in genetic techniques. However, there are discrepancies in the rate and success of detection of cryptic taxa between studies using genetic methods and those using classic external morphology analyses. Therefore, novel integrative methods for species delimitation of cryptic taxa provide an avenue to incorporate multiple lines of evidence, including the application of osteological variation assessment where external morphological assessment fails to distinguish species. I develop a new pipeline integrating genomic data using single nucleotide polymorphisms (SNPs) and osteological geometric morphometric evidence from micro X-ray computed tomography (CT) imagery to assess variation between cryptic lineages for confident species delimitation. i Here, I use this novel integrative pipeline to delimit cryptic lineages of earless dragons in north-eastern Australia. Prior to this study, there was evidence of three undescribed species of Tympanocryptis in this region. Using single mitochondrial and nuclear genes along with >8500 SNPs, I assess the evolutionary independence of the three target lineages and several closely related species. I then integrate these phylogenomic data with osteological cranial variation from CT imagery between lineages. I find that the very high levels of genomic differentiation between the three target lineages is also supported by significant osteological differences between lineages. By incorporating multiple lines of evidence for species delimitation, I provide strong support that the three cryptic lineages of Tympanocryptis in north-eastern Australia warrant taxonomic review. Earless dragons are found in most environments across the Australian continent, including a variety of ecological niches, from stony desert to tropical woodland or cracking clay savannah, although each species is often restricted to s certain habitat-type. I investigate the phylogenetic relationships among currently described earless dragons and newly delimited putative species with an assessment of broad biogeographic divisions, focussing on the north-eastern Australian Tympanocryptis group. I found significant structure across the north-eastern Australian lineages, with deep divergence between lineages occurring in the inland Great Artesian Basin region and more coastal Great Dividing Range. Regional diversification is estimated to have occurred in the late Miocene with subsequent Plio-Pleistocene speciations, and divergence and distributions of these species may therefore be reflective of the climate induced grassland-rainforest oscillations during this time. Based on these phylogenetic geographic relationships and the species delimitation from the integrative taxonomy approach, I describe three new species of Tympanocryptis from the cracking clay grasslands of the Darling Riverine Basin (T. darlingensis sp. nov.) and Queensland Central Highlands (T. hobsoni sp. nov.), and the ii stony open eucalypt woodlands on the Einasleigh Uplands (T. einasleighensis sp. nov.). The revision of these species provides further taxonomic clarity within the Tympanocryptis genus, and is an imperative step in the conservation of the north-eastern Australian earless dragons. These three putative Tympanocryptis species and the other three recently described earless dragons in north-eastern Australia inhabit restricted niches and areas with varying levels of habitat fragmentation and modification, and are therefore of significant conservation concern. However, little is known about these six north-eastern Australian earless dragon species. I utilise genomic methods to investigate population connectivity and genetic structure to determine management units. I then use species distribution modelling (SDM) to assess habitat suitability and fragmentation of each species. I integrate results of these analyses to form conclusions on the distribution and population structure of these earless dragons. I then discuss the major threatening processes and potential conservation strategies. This thesis uses several integrative approaches in resolving the taxonomy and forming conclusions on the conservation management of the north-eastern Australian Tympanocryptis species. This study successfully delimits cryptic lineages, explores the phylogenetic and geographic relationships between species, and provides baseline population genomics and ecological data to be used for conservation assessments and management decisions of earless dragons in north-eastern Australia. iii DECLARATION This is to certify that i) the thesis comprises only my original work towards the degree of the PhD except where indicated in the Preface; ii) due acknowledgement has been made in the text to all other material used; and iii) the thesis is fewer than 100,000 words in length, exclusive of tables, figures, bibliographies and appendices. Kirilee Chaplin 1st June 2018 iv PREFACE This thesis includes a series of independent chapters. Chapters 1-3 represent co- authored manuscripts for publication. Consequently, there may be some repetition between chapters. Although these manuscripts have been prepared in co-authorship, the contents of these chapters are my own work. Specific contributions of chapter co-authors are listed below. My supervisors Jane Melville and Joanna Sumner assisted with the development of the research questions and provided advice on the methodology and analyses of all chapters. Christy Hipsley advised on the osteological geometric morphometric approach in Chapter 1, and contributed to the analysis and interpretation of these data. Rod Hobson assisted with fieldwork and contributed conclusions for conservation management in Chapter 3. The conservation assessment for T. wilsoni in Appendix 1 was in collaboration with Melanie Venz. All co-authors commented on previous drafts of the manuscripts. This thesis includes the following chapters for publication: Chaplin K, Sumner J, Hipsley C, Melville J (in prep) A workflow pipeline for integrative species delimitation of cryptic taxa: a case study of earless dragon lineages in north- eastern Australian grasslands. Chaplin K, Sumner J, Melville J (in prep) Phylogenetic relationships of north-eastern Australian earless dragons (Agamidae: Tympanocryptis spp.), with description of three new species. Chaplin K, Sumner J, Hobson R, Melville J (in prep) Population genomics and species distribution modelling in conservation management of north-eastern Australian earless dragon lizards (Agamidae: Tympanocryptis spp.) v Appendix 1 includes the following Conservation Assessment submitted to and accepted by the Species Technical Committee of the Queensland Department of Environment and Heritage Protection: Venz M, Chaplin K (2016) Conservation assessment for Vulnerable listing of Roma earless dragon, Tympanocryptis wilsoni, under the Queensland Nature Conservation Act 1992 vi ACKNOWLEDGEMENTS I sit here writing this, still in disbelief that I have actually finally accomplished what I set out to do four years ago. I am incredibly proud of myself, and although there were several setbacks and challenges along the way with injury and illness, I made it to the finish line, with the support, assistance and care of many people along the way. I’d like to take a moment to appreciate and acknowledge some of those people who made this possible. Thankyou to my wonderful supervisors, Jane Melville and Jo Sumner. I really appreciate your input over the years in developing the project with me, helping me with the field or lab techniques, answering all of my questions and for all of your feedback and comments on the many drafts of the chapters of this thesis. Thanks for your support from the start to the very end, and I am so lucky to have had such amazing academic women as role-models and mentors during my postgraduate life. To three very special guys in my life: Trevor, Devon and Zafe. Trev, thankyou for inspiring me to do a
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