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Investigating the Loci That Contribute to Convergent Craniofacial Evolution Between the Thylacine and Canids

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Investigating the Loci That Contribute to Convergent Craniofacial Evolution Between the Thylacine and Canids Investigating the loci that contribute to convergent craniofacial evolution between the thylacine and canids Axel Newton 573760 ORCID ID: 0000-0001-7175-5978 Doctor of Philosophy July 2018 School of BioSciences, Faculty of Science, The University of Melbourne Melbourne Museum, Museums Victoria Submitted in total fulfilment of the requirements of the degree of Doctor of Philosophy i ii Abstract One of the most fundamental questions in evolutionary developmental biology is how phenotypic adaptations are controlled at the molecular level. One way we can address this question is by looking at examples of convergent evolution between distantly related species. Here we can ask the question; are similarities in morphology reflected by similarities in the genome? One of the most striking cases of convergent evolution in mammals is seen between the marsupial thylacine (or Tasmanian tiger) and placental canids (wolves, dingos and foxes) particularly in their cranial morphology. However, the extent of their morphological convergence has never been directly quantified. In my thesis I use a combination of morphological and molecular data to investigate candidate loci that may contribute to convergent craniofacial evolution between the thylacine and the canids. Using a geometric morphometric comparison of cranial shape between extinct and extant marsupial and placental mammals, I showed that the adult thylacine and canids represent a remarkable case of craniofacial convergence. By additionally CT scanning and landmarking all known thylacine pouch young specimens, I was able to demonstrate that the marsupial thylacine overcame its conserved neonatal constraints towards the end of its developmental period in the pouch. The strong similarities between the thylacine and canids are likely driven by underlying changes in cranial neural crest cells (NCCs), which are directly responsible for patterning the facial skeleton. I next investigated candidate loci that might be underpinning this extraordinary phenotypic convergence. RUNX2 is expressed in NCCs and is strongly implicated in driving facial length evolution in placental mammals. I hypothesized that similarities in the RUNX2 gene might partially explain similarities in facial shape between the thylacine and canids. However, unexpectedly, we found that the marsupials possess an invariant RUNX2 which cannot explain the diversity of facial shapes seen within marsupials nor craniofacial convergence. Instead, changes in facial length might be mediated through regulatory changes to RUNX2 expression. Using a genome-wide approach, we investigated homoplasy in protein coding genes. While overall homoplasy was extremely rare, we identified multiple thylacine/canid homoplasious amino acid substitutions in the osteogenic chromatin remodeller, CHD9, a known upstream regulator of RUNX2. We found that the amino acid substitution in the DNA binding domain resulted in differential expression and activation of RUNX2 in vitro and may act as a contributor to RUNX2-mediated craniofacial convergence. iii While I found evidence for changes in protein coding genes potentially contributing to convergence, the pleiotropic consequences of mutations in key developmental genes are thought to limit their evolvability. As such, we also used a genome wide approach to investigate accelerated evolution and convergence in the non-coding portion of the genome. We identified multiple putative cis-regulatory elements (CREs), including an enhancer upstream of the craniofacial TGF-β signalling receptor ACVR2A, also critical in NCCs. We found that the thylacine enhancer was able to drive craniofacial expression in the mouse and is a potential candidate mediating convergent craniofacial evolution. This finding suggests CREs may also play important roles in adaptive evolution and convergence. In this thesis I find support for protein coding and CRE evolution driving convergent craniofacial similarities. This supports my hypothesis that convergence targets genes and CREs in the NCCs directing craniofacial convergence between the thylacine and canids. iv Declaration This is to certify that: • This thesis is comprised of only my original work towards the requirements of the PhD, except where otherwise indicated. • I have given due acknowledgement in the text to all other materials used. • This thesis is less than 100,000 words in length, excluding tables, figures, references and appendices. Axel Newton School of BioSciences The University of Melbourne Victoria, 3010 Australia July 2018 v Preface This thesis contains an original introduction, five results chapters, a chapter addendum (Chapter 2) and a general discussion. Three chapters have been published in peer reviewed journals and 3 are formatted for future submission and publication. Chapter 2 presents an expanded analysis of material presented in Feigin et al., 2018, rewritten to highlight my geometric morphometric analyses and incorporating data from the supplementary materials. Chapter 6 uses data currently under consideration for publication at PNAS. Feigin, Newton and Pask, 2018 Chapter 2: Charles Y. Feigin, Axel H. Newton, Jürgen Schmitz, Liliya Doronina, Christy A. Hipsley, Kieren J. Mitchell, Graham Gower, Bastien Llamas, Julien Soubrier, Thomas N. Heider, Brandon R. Menzies, Alan Cooper, Rachel J. O’Neill & Andrew J. Pask, 2017, Genome of the Tasmanian Tiger Provides Insights into the Evolution and Demography of an Extinct Marsupial Carnivore Published by Nature Ecology & Evolution 30th August, 2017 and expanded C.Y.F. and A.J.P. conceived the study and wrote the manuscript with help from all co-authors. C.Y.F. performed genome assembly and comparative genomic analyses. A.H.N. and C.A.H. performed morphometric analyses. J.Schmitz performed retrophylogenomic data analyses. L.D. performed retrophylogenomic analyses and experimental screening of retroposon presence/absence patterns. J.Soubrier, B.L., K.J.M. and G.G. performed MSMC and mapDamage analyses. A.C. assisted in interpreting the latter, and manuscript writing. T.N.H. performed identification of X scaffolds. B.R.M. performed sample sourcing and collection. R.J.O. assisted with sequencing strategy. Chapter 3: Axel H. Newton, Frantisek Spoutil, Jan Prochazka, Jay R. Black, Kathryn Medlock, Robert N. Paddle, Marketa Knitlova, Christy A. Hipsley, Andrew J. Pask, Letting the ‘cat’ out of the bag: vi pouch young development of the extinct Tasmanian tiger revealed by X-ray computed tomography Published by Royal Society Open Science 21st February 2018. A.H.N., C.A.H. and A.J.P. designed and conceived the study, and wrote the manuscript. M.K. allowed access to Prague specimens. F.S. performed scanning, reconstruction, postprocessing, morphological and morphometrical analysis of Prague specimens. J.R.B. performed scanning, reconstruction and postprocessing of all Australian specimens. A.H.N. performed morphometric and statistical analyses on complete series. K.M. and R.N.P. contributed historical and biological information. All authors reviewed and revised the manuscript, and gave final approval for publication. Chapter 4: Axel H Newton, Charles Y Feigin, Andrew J Pask, RUNX2 repeat variation does not drive craniofacial diversity in marsupials Published by BMC Evolutionary Biology 4th May 2017 All authors conceived and designed the project. AHN and C.Y.F collected and analysed the data. A.H.N and A.J.P wrote the paper. All authors edited the manuscript. All authors read and approved the final manuscript. Chapter 5: Axel H Newton & Andrew J Pask, Evolutionary amino acid substitutions in the DNA binding domain of CHD9 alter the expression of RUNX2 Unpublished material not submitted for publication. vii Chapter 6: Axel H Newton, Charles Y Feigin & Andrew J Pask, Convergent accelerated evolution of an ACVR2A enhancer in the thylacine and canids reveals a novel candidate driver of craniofacial evolution Unpublished material not submitted for publication. Data used from Charles Y Feigin, Axel H Newton & Andrew J Pask, Comparative Genomics Identifies Widespread Cis-Regulatory Convergence Between the Extinct Tasmanian Tiger and Grey Wolf. Under consideration at PNAS 2018. viii Acknowledgements This whole journey started when faced with a predicament after returning from two years travelling around North America. With something along the lines of “what on earth do I do now..?”, I looked into restoring my passion for science through yet another university course. After successfully completing an undergrad and honours degree at Deakin University, the next logical step to prolonging my student status was to enrol in a masters degree. Which degree? Well something at the University of Melbourne seemed a good choice, given their reputation. As such I found the Master of Biotechnology, which in hindsight was nothing like I had pictured, however it was this degree that formed the foundations for the last 3 and a half years of my life as a PhD candidate. This is where my acknowledgements begin. First and foremost, Dr. Matthew Digby, the co- ordinator of the Master of Biotechnology degree, took a reasonably unorthodox and unique approach to his workshops and teaching styles, even allowing us to watch the movie “The Internship” to examine workplace do and don’ts... One day Digby told us to write a short essay detailing our interests, a specific goal, and a 5 year plan on how to achieve this. I was always fascinated with the prospects of cloning and genetic engineering (hence the biotechnology), almost entirely thanks to Jurassic park and Gattaca,
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