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Thomas Mutton Thesis EVOLUTIONARY BIOLOGY OF THE AUSTRALIAN CARNIVOROUS MARSUPIAL GENUS ANTECHINUS Thomas Yeshe Mutton B. App. Sci. (Hons) School of Earth, Environmental and Biological Sciences Science and Engineering Faculty Queensland University of Technology Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy i Keywords Antechinus, Australia, Australian mesic zone, biogeographical barriers, biogeography, breeding biology, congeneric competition, conservation, genetic structure, Dasyuridae, dasyurid, life-history, mammal, mammalian, Miocene, molecular systematics, Phascogalini, phylogenetics, phylogeography, Pleistocene, Pliocene, population genetics, Queensland, systematics (Davison ) ii Abstract Antechinus is an Australian genus of small carnivorous marsupials. Since , the number of described species in the genus has increased by % from ten to fifteen. The systematic relationships of these new species and others in the genus have not been well resolved and a broad phylogeographic study of the genus is lacking. Moreover, little ecological information is known about these new species. Therefore, the present study examined the evolutionary biology of Antechinus in two complimentary components. The first component aimed to resolve the systematics and phylogeography of the genus Antechinus. The second component, at a finer spatiotemporal scale, aimed to improve understanding of the autecology, habitat use and risk of extinction within the group, with a focus on the recently named buff-footed antechinus, A. mysticus and a partially sympatric congener, A. subtropicus. To date, powerful (>two gene) molecular studies have only included eight Antechinus species. Here, the first comprehensive, multi-gene phylogenetic analysis of the genus using six genes was provided, incorporating all known species and subspecies of Antechinus. Four main lineages of Antechinus were reconstructed: () The dusky antechinus (A. arktos, A. swainsonii, A. vandycki, A. mimetes) and A. minimus; () A. godmani; () A. agilis, A. stuartii and A. subtropicus; () A. argentus, A. mysticus, A. adustus, A. flavipes, A. leo and A. bellus. The inclusion of A. adustus in lineage was surprising, as it was previously believed a member of lineage . One species, A. stuartii, was not monophyletic and may be more appropriately classified as two species. Timing of cladogenesis was estimated for all species of Antechinus, permitting an evolutionary scenario to be posited for the group. The mesic zone is the ancestral biome of Australia and, by most measures, the zone of highest taxonomic diversity. However, the south-east region of the iii zone has been identified as lacking in mammalian phylogeographic studies. Sequencing of the mitochondrial Cytochrome-b (Cytb) gene was therefore undertaken broadly throughout the geographic range of all species of Antechinus, which collectively occur across the entire zone. High levels of intraspecific phylogeographic structure, largely corresponding to probable Pleistocene biogeographic barriers and comparable to the genetic divergence between named Antechinus subspecies, were revealed in a number of species. For example, the broadly distributed A. flavipes flavipes contained two divergent clades which appear to have been separated by the Great Dividing Range. Within the south-east Australian A. agilis, four phylogeographic clades were identified, each of which appears to have been divided by putative biogeographic barriers. Antechinus mimetes mimetes showed strong divergence between north-east NSW and southern populations. Victorian populations of this species also appear to have been divided by the East Gippsland Basin which may also have divided A. agilis clades and other taxa in the region. Considerable divergence was found between south-east Queensland populations of A. mysticus and the only known population in mid- east Queensland. The buff-footed antechinus, A. mysticus, was only recently discovered and consequently it is not well understood. It has been suggested that this species utilises a broad range of habitats which over time may result in highly connected populations at a regional scale. This hypothesis was tested using a population genetic approach. Nine microsatellite loci were genotyped for six populations of A. mysticus, sampled from throughout its known range (Eungella in mid-east Qld [ME Qld] and south-east Qld [SE Qld]). Comparative data were sought from four populations of A. subtropicus, which can occur in sympatry across a similar area of SE Qld. Antechinus subtropicus is known to utilise altitudinal vine and rainforest communities which are more fragmented; consequently, it was expected to show greater population differentiation than A. mysticus. Two populations of A. mysticus were revealed to be deeply divergent from most SE Qld populations examined: Eungella (ME iv Qld), which is in geographic isolation (>km) from the other A. mysticus populations, and Cooloola (SE Qld). Cooloola is the northernmost known SE Qld population of A. mysticus and shares a mtDNA Cytb haplotype with other SE Qld populations. Yet this population had low microsatellite allelic diversity and appears to be in very low abundance, suggesting divergence is driven by population isolation; it may be at extinction risk. Genetic structure between the other SE Qld populations was also higher than expected, similar to A. subtropicus populations. This suggests A. mysticus is patchily distributed and may be limited to moderate altitude and wetter environments in SE Qld. The first multi-year ecological study of breeding, growth and movement of A. mysticus was also undertaken. Over a two year period, monthly capture-mark- recapture data from two proximate (~.km apart) sites were collected. At one site, the subtropical antechinus, A. subtropicus, occurred in sympatry. Antechinus mysticus followed the synchronous semelparous (suicidal breeding) breeding strategy seen in all Antechinus. Males were last caught in August at both sites and females appear to give birth in September. Average movement by A. mysticus was comparable to other similar-sized congeners. Antechinus subtropicus occurred at lower density although not lower body mass than proximate conspecifics, at this relatively low altitude study site. Competition from A. subtropicus may affect A. mysticus, as A. mysticus have a higher body mass and males moved further when not in sympatry with A. subtropicus. Taken together, the present study permitted an investigation of spatio- temporal influences on Antechinus evolution, from the distant Miocene to a very recent inter-generational scale. Genetic diversity was found to be high in Antechinus at all levels investigated which suggests this mesic genus has experienced fragmentation throughout its existence. Several Antechinus species are at risk of extinction. In light of the observed population structuring and purported history of fragmentation, Antechinus must be closely monitored v in a future likely to include further habitat degradation, as temperatures and human abundance increases across Australia. vi Table of Contents Keywords ................................................................................................................................. ii Abstract ................................................................................................................................... iii Table of Contents ................................................................................................................... vii List of Figures ......................................................................................................................... ix List of Tables ........................................................................................................................ xiii Statement of Original Authorship ......................................................................................... xvi Acknowledgements .............................................................................................................. xvii Chapter 1: General introduction ................................................................................................ 1 1.1 Taxonomy and systematics of Antechinus ...................................................................... 1 1.2 Biogeography.................................................................................................................. 3 1.3 Life history and breeding biology .................................................................................. 4 1.4 Movement and home-range ............................................................................................ 6 1.5 The present study ............................................................................................................ 7 Chapter 2: Molecular systematics and evolution of the genus Antechinus .. 11 2.1 Introduction .................................................................................................................. 12 2.2 Materials and methods .................................................................................................. 16 2.3 Results .......................................................................................................................... 22 2.4 Discussion ..................................................................................................................... 31 Chapter 3: Phylogeography of the genus Antechinus ..................................... 39 3.1 Introduction .................................................................................................................
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