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Psmissen Phd Thesis Evolutionary biology of Australia’s rodents, the Pseudomys and Conilurus Species Groups Peter J. Smissen Submitted in total fulfilment of the requirements of the degree of DOCTOR OF PHILOSOPHY May 2017 School of BioSciences Faculty of Science University of Melbourne Produced on archival quality paper 1 Dedicated to my parents: Ian and Joanne Smissen. 2 Abstract The Australian rodents represent terminal expansions of the most diverse family of mammals in the world, Muridae. They colonised New Guinea from Asia twice and Australia from New Guinea several times. They have colonised all Australian terrestrial environments including deserts, forests, grasslands, and rivers from tropical to temperate latitudes and from sea level to highest peaks. Despite their ecological and evolutionary success Australian rodents have faced an exceptionally high rates of extinction with >15% of species lost historically and most others currently threatened with extinction. Approximately 50% of Australian rodents are recognised in the Pseudomys Division (Musser and Carleton, 2005), including 3 of 10 historically extinct species. The division is not monophyletic with the genera Conilurus, Mesembriomys, and Leporillus (hereafter Conilurus Species Group, CSG) more closely related to species of the Uromys division to the exclusion of Zyzomys, Leggadina, Notomys, Pseudomys and Mastacomys (hereafter Pseudomys Species Group, PSG). In this thesis, I resolved phylogenetic relationships and biome evolution among living species of the PSG, tested species boundaries in a phylogeographically-structured species, and incorporated extinct species into a phylogeny of the CSG. To resolve phylogenetic relationships within the Pseudomys Species Group (PSG) I used 10 nuclear loci and one mitochondrial locus from all but one of the 33 living species. The group comprises five genera, which are widely distributed across the continent’s biomes, and represent the most 3 diverse group of rodents to evolve from a single colonization of Australia. With a well-resolved phylogeny I recovered limited support for an early burst in diversification, instead indicating a steady continuous rate of diversification through time. I identify and date at least 14 biome transitions since the group’s origin 5-8 Mya, with early transitions between the monsoon and arid biomes, but with transitions into the temperate mesic biome occurring ~2 MY later. I found that early-evolving genera specialised to individual biomes with few transitions to other biomes, where the phylogenetically-nested genus Pseudomys transitioned between arid and mesic biomes repeatedly. My results suggest that at the broad environmental scale of biome transitions evolutionarily labile niche divergence can evolve in lineages descended from niche-conservative taxa. Within the endangered Hastings River mouse, Pseudomys oralis, I tested if geographically-structured mitochondrial lineages reflect distinct species by sequencing nine independent nuclear exons. Pseudomys oralis is distributed along the eastern mesic zone of Australia across the Macleay-Mcpherson Overlap Zone (MMOZ) in northern New South Wales. This suture zone represents the contact between divergent northern and southern lineages from several taxa driven by the interplay between its biogeographic barriers and Pleistocene climatic fluctuations. Pseudomys oralis is comprised of two mitochondrial lineages that are distributed in the northern and southern parts of its range, and overlap in MMOZ. Using nine nuclear exons I showed the deep divergence between mitochondrial lineages is not reflected in the nuclear genome. I recovered limited differences in allele frequencies of 4 nuclear exons among mitochondrial lineages with a zone of overlap at Washpool National Park, NSW. However, gene flow between these two populations is most consistent with panmixia, suggesting that the populations are freely interbreeding and do not reflect distinct species. Overall, Pseudomys oralis exhibit a pattern of shallow divergence with recent secondary contact. This pattern is consistent with isolation and secondary contact resulting from Pleistocene contraction and fragmentation of east coast mesic forests as reported for other taxa in this region. To resolve phylogenetic relationships in the Conilurus Species Group (CSG) including placement of the extinct species, Conilurus albipes, I developed a custom in-solution based target enrichment system that targets 1366 nuclear exons and two mitochondrial protein-coding genes. I developed the system to capture and sequence genomic-scale data from both recent tissues and historical skins. The CSG comprises three genera and seven species, three of which have been lost to extinction historically. I sequenced 1368 exonic regions from all 4 living species of the CSG and from one extinct species, the White-footed Rabbit-rat, Conilurus albipes, represented by an historical museum skin collected in the 1850s. I used replicate DNA extractions for the skin specimen to demonstrate high accuracy and limited DNA damage for 349 of 1368 loci. I placed C. albipes in a phylogeny with its congener C. penicillatus, as well as 11 other species of Australian rodents, and dated their divergence to 2.5 Mya, a comparably deep divergence compared to other sister taxa like Mesembriomys gouldii and M. macrourus, and Pseudomys australis and Mastacomys fuscus. 5 My thesis revealed the rapid diversification, biome transitions, population structure, and loss of genomic diversity through extinction in Australian rodents. I highlight this group as a unique opportunity to investigate questions across numerous areas including: phylogeography, population genetics, conservation, convergence and adaptive evolution, colonisations and biome transitions, extirpation and extinction, and diversification and species delimitation. Australia’s rodent fauna represents an important model system for answering numerous questions across the broad field of evolutionary biology. 6 Declaration This is to certify that: i) This thesis comprises only my original work towards the degree of PhD; 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, maps, bibliographies and appendices. Peter J. Smissen May 2017 7 Preface This thesis comprises a series of independent publications. Chapters 2-4 include co-authored manuscripts that have either been published or will be submitted for publication. Although the publications are co-authored, I performed the majority of laboratory work and analyses. I was also involved in fieldwork and museum visits in order to collect tissue for some specimens. Specific contributions of each co-author are outlined below. My supervisor Kevin Rowe assisted with the development of research questions and provided direction regarding methodology and analyses for each chapter. Tissues used in all chapters were collected from Museum Victoria, South Australia Museum and the Australia Biological Tissue Collection, and Southern Cross University. Emily Roycroft, Adnan Moussalli and Andrew Hugall aided in analyses in Chapter 4. Kevin Rowe carried out the library preparation for Chapter 4 at the Australian National University in conjunction with the Moritz Laboratory where the libraries for each samples were sequenced. All co-authors commented on previous drafts of the manuscripts. This thesis includes the following chapters for publication: Smissen, P. J., Rowe, K. C. (in review, March 2017) Reversible evolution of biome transitions in the recent evolution of Australian rodents 8 Smissen, P. J., Rowe, K. C. (in prep) Mito-nuclear discordance in the Hastings River Mouse, Pseudomys oralis, suggests dynamic population contraction-expansions during glacial cycles Smissen, P. J., Roycroft, E. J., Moussalli, A., Rowe, K. C. (in prep) Sequencing historic museum specimens of the extinct White-footed Rabbit-rat, Conilurus albipes, shows extensive diversity lost to extinction. 9 Acknowledgements This thesis was completed through the support of many different people. First and foremost, I want to thank my supervisor Kevin Rowe. Thank you for your continued support and confidence in my abilities, as well as helping me make sense of what was often confusing to interpret results, and also reading countless drafts of my thesis. I would like to thank the students and staff at Museum Victoria, particularly Kirilee Chaplin, Stella Shipway, Kate Trewin, Monique Winterhoff, Heru Handika, Karen Rowe, Rebecca Laver, Stella Claudius, and Mark Norman. I want to thank Andrew Hugall for his many insightful conversations as well. I also want to thank Joanna Sumner (Museum Victoria) and Stephen Donnellan (South Australian Museum) for generously providing tissue samples used in this thesis. Furthermore, I want to thank Craig Moritz (The Australian National University) and his laboratory for generously providing funding and helping with the library preparation and sequencing of specimens. Thank you so much Emily Roycroft and Phoebe Burns. Thanks for the endless hours of support and debauch. You guys kept me sane all along this long road to the end. I can’t thank you guys enough and wish you all the best with your PhDs and future careers. 10 I would also like to thank my family. Thank you to Annika Smissen and Rory Douglas, and to my parents Ian and Joanne Smissen. You both instilled in me an endless amount of curiosity and passion for the natural world from a very young age. Without your constant support and
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