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Tarantulas of Australia: Phylogenetics and Venomics Renan Castro Santana Master of Biology and Animal Behaviour Bachelor of Biological Sciences

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Tarantulas of Australia: Phylogenetics and Venomics Renan Castro Santana Master of Biology and Animal Behaviour Bachelor of Biological Sciences Tarantulas of Australia: phylogenetics and venomics Renan Castro Santana Master of Biology and Animal Behaviour Bachelor of Biological Sciences A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2018 School of Biological Sciences Undescribed species from Bradshaw, Northern Territory Abstract Theraphosid spiders (tarantulas) are venomous arthropods found in most tropical and subtropical regions of the world. Most Australian tarantula species were described more than 100 years ago and there have been no taxonomic revisions. Seven species of theraphosids are described for Australia, pertaining to four genera. They have large geographic distributions and they exhibit little morphological variation. The current taxonomy is problematic, due to the lack of comprehensive revision. Like all organisms, tarantulas are impacted by numerous environmental factors. Their venoms contain numerous peptides and organic compounds, and reflect theraphosid niche diversity. Their venoms vary between species, populations, sex, age and even though to maturity. Tarantula venoms are complex cocktails of toxins with potential uses as pharmacological tools, drugs, and bioinsecticides. Although numerous toxins have been isolated from venoms of tarantulas from other parts of the globe, Australian tarantula venoms have been little studied. Using molecular methods, this thesis aims to document venom variation among populations and species of Australian tarantulas and to better describe their biogeography and phylogenetic relationships. The phylogenetic species delimitation approach used here predicts a species diversity two to six times higher than currently recognized. Species examined fall into four main clades and the geographic disposition of those clades in Australia seems to be related to precipitation and its seasonality. Australian tarantulas are shown to be non- monophyletic. Species may have immigrated multiple times between South-east Asia (SEA) and Australia. Australian species belonging to the genera Phlogius and Coremiocnemis are shown to be paraphyletic. However, the inclusion of “true” Selenocosmia species, e.g., from southeast Asia, is necessary to make more sound decisions regarding synonyms and diagnoses. Haplotypes of P. crassipes reveals highly genetically structured genes and the absence of isolation by distance. Phlogius crassipes is composed of at least two cryptic species, and here its range and diagnosis are updated. Phlogius strenuus is transferred from Selenocosmia and its range and diagnosis are updated. With the new range of Phlogius strenuus, it is clear that populations, genetic diversity, and even entire species are at risk, based upon the assumption that the species might be harvested sustainably is rejected. I found 26 phylogenetic clades using 2% divergence of the nucleotides of the 16S barcode region. Using whole venom profiling, the venom of individuals within a clade varies as much as across clades. However, venom belonging to phylogenetic groups contained at least one unique peptide that could be utilised to distinguish it from other phylogenetic groups. These results suggest that venom variation between phylogenetic groups may be useful in ascertaining species identity. I show that the venom of P. strenuus changes continuously during development and throughout adulthood, i.e., there are ontogenetic changes in venom composition. Intraspecific and interspecific venom variation can demonstrate how fast evolving and adaptive venom can be. The presence of unique peptides within each phylogenetic group is evidence that the specificity of venom could be used as an identification method in future. In addition, unique peptides within potential species and within each maturity stage present extra evidence that a single species can highly contribute to amplify our chemical library, which can increase possibilities of making new pharmacological discoveries. Declaration by author This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, financial support and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my higher degree by research candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis and have sought permission from co-authors for any jointly authored works included in the thesis. Publications during candidature Santana, R. C., Perez, D., Dobson, J., Panagides, N., Raven, R. J., Nouwens, A., Jones, A., King, G. F., Fry, B. G. (2017). Venom profiling of a population of the theraphosid spider Phlogius crassipes reveals continuous ontogenetic changes from juveniles through adulthood. Toxins, 9(4), 116. https://doi.org/10.3390/toxins9040116 Santana, R. C. (2015). Community structure and composition of litter spiders (Arachnida: Araneae) and influence of macro-climatic factors on Parque Ecológico Jatobá Centenário, Morrinhos, Goiás, Brazil. Journal of Threatened Taxa, 7(10), 7612–7624. https://doi.org/10.11609/JoTT.o4030.7612-24 Publications included in this thesis Santana, R. C., Perez, D., Dobson, J., Panagides, N., Raven, R. J., Nouwens, A., Jones, A., King, G. F., Fry, B. G. (2017). Venom profiling of a population of the theraphosid spider Phlogius crassipes reveals continuous ontogenetic changes from juveniles through adulthood. Toxins, 9(4), 116. https://doi.org/10.3390/toxins9040116 – incorporated as Chapter 5. Contributor Statement of contribution Renan Castro Santana (Candidate) Conception and design (50%) Analysis and interpretation (50%) Drafting and production (57%) David Perez Conception and design (0%) Analysis and interpretation (4 %) Drafting and production (1%) James Dobson Conception and design (0%) Analysis and interpretation (4%) Drafting and production (3%) Nadia Panagides Conception and design (0%) Analysis and interpretation (4%) Drafting and production (3%) Robert J. Raven Conception and design (5%) Analysis and interpretation (10%) Drafting and production (10%) Amanda Nouwens Conception and design (5%) Analysis and interpretation (4%) Drafting and production (3%) Alun Jones Conception and design (10%) Analysis and interpretation (4%) Drafting and production (3%) Glenn F. King Conception and design (15%) Analysis and interpretation (10%) Drafting and production (10%) Bryan G. Fry Conception and design (15%) Analysis and interpretation (10%) Drafting and production (10%) Manuscripts included in this thesis None Contributions by others to the thesis Chapter one: Dr Robert J. Raven – editing draft. Dr Bryan G. Fry – editing draft. Dr Lyn Cook – editing draft. Chapter two: Dr Robert J. Raven – financial support for DNA sequencing, assisted with field collection and editing draft. Dr Bryan G. Fry – financial support for DNA sequencing. Dr Lyn Cook – financial support for DNA sequencing, assisted creating ideas, analysis of data and draft dediting to end of section. Dr Jason Bond – financial support for DNA sequencing. Ethan Briggs – assisted with field collection and laboratory work. Chapter three: Dr Robert J. Raven – financial support for DNA sequencing, assisted field collection, creating ideas and draft edition. Dr Bryan G. Fry – financial support for DNA sequencing. Dr Lyn Cook – financial support for DNA sequencing, assisted creating ideas, analysis of data and draft edition. Chapter four: Dr Robert J. Raven – financial support for DNA sequencing and assisted with draft edition. Dr Bryan G. Fry – financial support for DNA sequencing and venom proteomics, assisted with draft edition. Dr Lyn Cook – financial support for DNA sequencing, assisted creating ideas, analysis of data and draft edition. Kimberley Biggs – assisted with data analysis and draft production. Dr Simon Blomberg – assisted with statistical analysis. Dr Alun Jones – assisted with mass spectrometry runs and analysis. Chapter five: Contributions listed under section “Publications included in this thesis” Statement of parts of the thesis submitted to qualify for the award of another degree None Research Involving Human or Animal Subjects None Acknowledgements Firstly, I would like to thank my supervisors, Dr Robert Raven, Dr Lyn Cook, Associate Professor Bryan Fry and Professor Glenn King, for all support and mentoring during the course of this study. Their indispensable
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