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On the Evolution of Kangaroos and Their Kin (Family Macropodidae) Using Retrotransposons, Nuclear Genes and Whole Mitochondrial Genomes

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On the Evolution of Kangaroos and Their Kin (Family Macropodidae) Using Retrotransposons, Nuclear Genes and Whole Mitochondrial Genomes ON THE EVOLUTION OF KANGAROOS AND THEIR KIN (FAMILY MACROPODIDAE) USING RETROTRANSPOSONS, NUCLEAR GENES AND WHOLE MITOCHONDRIAL GENOMES William George Dodt B.Sc. (Biochemistry), B.Sc. Hons (Molecular Biology) Principal Supervisor: Dr Matthew J Phillips (EEBS, QUT) Associate Supervisor: Dr Peter Prentis (EEBS, QUT) External Supervisor: Dr Maria Nilsson-Janke (Senckenberg Biodiversity and Research Centre, Frankfurt am Main) Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy Science and Engineering Faculty Queensland University of Technology 2018 1 Keywords Adaptive radiation, ancestral state reconstruction, Australasia, Bayesian inference, endogenous retrovirus, evolution, hybridization, incomplete lineage sorting, incongruence, introgression, kangaroo, Macropodidae, Macropus, mammal, marsupial, maximum likelihood, maximum parsimony, molecular dating, phylogenetics, retrotransposon, speciation, systematics, transposable element 2 Abstract The family Macropodidae contains the kangaroos, wallaroos, wallabies and several closely related taxa that occupy a wide variety of habitats in Australia, New Guinea and surrounding islands. This group of marsupials is the most species rich family within the marsupial order Diprotodontia. Despite significant investigation from previous studies, much of the evolutionary history of macropodids (including their origin within Diprotodontia) has remained unclear, in part due to an incomplete early fossil record. I have utilized several forms of molecular sequence data to shed light on the phylogeny and the timescale of kangaroo evolution. This was carried out at the family level (Macropodidae), by investigating the genera Macropus, Wallabia, Lagorchestes, Onychogalea, Setonix, Lagostrophus, Dorcopsis, Dorcopsulus, Thylogale, Dendrolagus and Petrogale, and at the genus level, by investigating the relationships among the species of Wallabia and Macropus (which contain many of the most iconic species, including the largest living marsupials), and in turn, the relationships among the three sub-genera of Macropus – M.(Macropus), M. (Osphranter) and M. (Notmacropus). This study expands traditional molecular data matrices for mitochondrial genomes and nuclear genes, and I present the first retrotransposon-based phylogeny of kangaroos, utilizing a dataset of 29 phylogenetically informative retrotransposon markers that shed light on several contentious relationships among kangaroos. Maximum parsimony retrotransposon analysis shows that the enigmatic swamp wallaby (Wallabia bicolor) has a close relationship with the forest wallabies of the Macropus subgenus, Notamacropus, thus necessitating taxonomic revision of the genera Macropus and Wallabia. The black gloved wallaby (M. irma) groups with the wallabies of Macropus (Notamacropus), which conflicts with previous mitochondrial analyses that place it within Macropus (Osphranter). I find moderate support from retrotransposons for grouping the nail tail wallabies as the sister group to Macropus/Wallabia - a finding that is not supported by any other molecular analysis, but has been suggested, based on morphology. 3 In addition, I have addressed an ascertainment bias that arises in retrotransposon studies that utilize only a single reference genome and I present a new statistical framework that addresses this ascertainment bias. Furthermore, the detection of polymorphic retrotransposon insertions in M. eugenii suggests that there has been very recent activity of a particular retrotransposon family (KERV) in the kangaroo genome, while another retrotransposon (LINE1) appears to have become silenced, hinting at the possibility of competition between these elements in the genome. This phenomenon has been observed in only a small number of other taxa and has implications for understanding genome evolution in macropods. Next, the taxonomic depth of phylogenetic inference was increased for a dataset that includes mitochondrial genomes and five nuclear genes, both through new sequencing and previously unpublished data within the lab group. This includes the first phylogenetically informative DNA sequences from the elusive black wallaroo (M. bernardus) and the first DNA sequence from the extinct toolache wallaby (M. greyi). This is the first molecular study of kangaroos to provide complete taxon sampling, covering all living members (and one recently extinct member), of the genera Macropus and Wallabia. I analysed the mitochondrial and nuclear genes separately, as well as in a combined ‘supermatrix’ dataset consisting of 21,278 bp of concatenated sequence data. Notably, I find M. bernardus is the deepest diverging of the wallaroos within M. (Osphranter), while the extinct toolache wallaby (M. greyi) groups within M. (Notamacropus) as sister to M. irma. The evolutionary history of kangaroos was explored using molecular dating, a lineage through time analysis and ancestral state reconstructions of key phenotypic traits - habitat preference, mob size and sexual dimorphism for size and colour. Ancestral reconstructions inferred that multiple transitions from closed/wet forest environments into more arid zones are coincident with the cooling/drying of Australia since the mid-Miocene climatic optimum, 15 – 16 Ma. I show that large mob size and sexual dimorphism tends to be more pronounced in species with ranges that have expanded into more arid grasslands, and that sexual dimorphism appears to be primarily male-driven. 4 Finally, looking deeper in the macropodid tree, I investigated the relationships and timing among the genera within the Macropodidae in order to shed light on the current six-way polytomy between Macropus/Wallabia, Lagorchestes, Onychogalea, Setonix, Dorcopsis/Dorcopsulus, Dendrolagus/Petrogale/Thylogale. I sequenced and analysed six novel nuclear genes and combined these with five nuclear genes from a previous study and also with complete and partial mitochondrial genomes. I recovered a strong affinity between Lagorchestes and Macropus/Wallabia, with Setonix and Onychogalea sitting consecutively further out. Sister to this clade was a clade containing the Dendrolagini (Dendrolagus and Petrogale) and Thylogale, with the Dorcopsini (Dorcopsis and Dorcopsulus) as the deepest diverging lineage in this clade. The timing of the major divergences appears to have taken place after the mid- Miocene climatic optimum as the climate continued to become cooler and more arid. 5 Table of contents Keywords ................................................................................................................................................ ii Abstract.................................................................................................................................................. iii Table of contents ................................................................................................................................... vi List of Figures ......................................................................................................................................... x List of Tables ....................................................................................................................................... xiii List of abbreviations ............................................................................................................................. xv Statement of original authorship .......................................................................................................... xvi Acknowledgments .............................................................................................................................. xvii CHAPTER 1: INTRODUCTION........................................................................................................ 1 1.1 Purpose ........................................................................................................................................ 1 1.2 Background and Context - Literature Review ............................................................................. 2 1.2.1 Marsupials ........................................................................................................................ 2 1.2.2 Kangaroos and their kin ................................................................................................... 6 1.2.3 Phylogenetic Reconstruction Using Molecular Sequence Data ..................................... 13 1.2.4 Molecular Phylogenies Using Transposable Elements .................................................. 17 1.2.5 Adaptive Radiations ....................................................................................................... 28 1.2.6 Reconstructing Evolutionary History Through Molecular Dating ................................. 30 1.2.7 Ancestral State Reconstruction ...................................................................................... 32 1.3 Objectives and thesis outline ..................................................................................................... 32 1.3.1 Chapter 1. Introduction .................................................................................................. 32 1.3.2 Chapter 2. Examining the phylogeny of the genus Macropus and Wallabia using retrotransposon insertions. ....................................................................................................................... 32 1.3.3 Chapter 3. Examining the phylogeny and timing of Macropus and Wallabia, utilizing nuclear genes and mitochondrial
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