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The Application of Molecular Genetics to the Conservation

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The Application of Molecular Genetics to the Conservation Management of Quolls, Dasyurus Species (Dasyuridae:Marsupialia) Karen B. Firestone Ph. D. Submitted December 1999 Abstract: The quolls are among the largest of the remaining carnivorous marsupials in the Australasian region, and thus occupy an important ecological niche as top predators and scavengers. All quolls are currently in decline and threatened to some degree yet the application of molecular information to the conservation and management of quolls has been unexplored until now. In this thesis I use two independent and highly variable genetic marker systems, the mitochondrial DNA (mtDNA) control region and nuclear microsatellites, to explore various aspects of conservation genetics relevant to the management of quolls. These aspects include an examination of the phylogenetic or evolutionary relationships among all six species of quolls, an examination of the genetic diversity within populations and the degree of differentiation between populations of the four Australian species of quolls, and the definition of units for conservation within these species. The development of suitable nuclear markers was a vital first step in defining levels of genetic variability and differentiation within and between the different populations and species. These markers proved to be highly variable and provided a wealth of information of relevance to the conservation of these species, and will be extremely useful in further studies. The use of the mtDNA control region for phylogenetic analyses was a novel approach to examining this question in quolls and also proved to be highly informative. Results from these phylogenetic analyses highlight the necessity of 1) examining more than one exemplar of each species, as well as 2) finally bringing some consensus to the question of the evolutionary relationships among quolls. Results show that northern quolls form the earliest split from all other quolls and that western quolls are closely related to the two New Guinean species. ii Furthermore, there is evidence for distinct lineages within species, corresponding to geographically separate or isolated populations. Levels of genetic variability within populations were examined using the microsatellites developed previously. Genetic variation was significantly higher in western quolls than in any other species. This was surprising given the long term and widespread decline of this species. There were also significant differences between populations within species in the level of genetic variability. Low levels of variability were usually found in small or captive bred populations or populations in severe decline. Genetic differentiation between populations was also explored using microsatellites. Significant differentiation in allele frequency distributions was found between most pairwise population comparisons, indicating that each of these populations forms a separate management unit (MU) for conservation purposes. One notable exception was found among populations of tiger quolls from a highly localized area in the Barrington Tops region of New South Wales. Using microsatellites, these populations were not significantly subdivided and thus appeared to be one MU. Using mtDNA, however, these populations were significantly subdivided and thus should be considered separate MUs. Differences in the way these two genetic markers are inherited (mtDNA is maternally inherited, microsatellites are biparentally inherited) provides a clue as to the social structure and organization of these cryptic nocturnal species. Consequently, the use of different genetic marker systems shows that there is sex-biased migration within this species. iii Finally, the degree of genetic differentiation observed within tiger quolls does not conform to the currently recognized subspecific categories within this species. The major genetic split occurs between the Tasmanian and mainland populations of tiger quolls, not between Dasyurus maculatus maculatus and D. m. gracilis. Thus, the Tasmanian and mainland populations form two distinct evolutionarily significant units (ESUs) for conservation purposes, and I propose that the Tasmanian populations should be elevated to the subspecific status to account for this. iv Table of Contents Abstract ......................................................................................................................................................................... 11 Table of Contents ............................................................................................................................................. v Acknowledgments .............................................................................................................................................. viii List of Figures ... ...................................................................................................................................................... xiii List of Tables ............................................................................................................................................................ xv Chapter 1. Introduction, Background, and Theoretical Framework ................................................................................................................................................................. 1 Organization of This Thesis ..................... ......................................... ...... ............................................................ ... 1 Description of Quolls ....................................................................................... ........................................................... 1 History of European Discovery, Nomenclature, and Taxonomic Status ofQuolls ........ 5 Fossil Dasyures ........ ................... ............. ................... ........ .... .................. ...... .... ... ... ............................... ............ .......... 9 Current Classification of the Dasyures .................... .............................. ........................................................ 1 0 Conservation Status ..................................................................................................................................................... 11 Population Declines, Range Contractions, and Current Distribution of Quolls ................ 13 Eastern Quoll, Dasyurus viverrinus ................................................................................................ 14 Tiger Quoll, Dasyurus maculatus .................................................................................................... 1 7 Western Quoll, Dasyurus geoffroii ................................................................................................. 20 Northern Quoll, Dasyurus hallucatus ........................................................................................... 22 Conservation Biology ......................................................... ....................................................................................... 23 Molecular Genetics in Conservation ......................... .............................................................. ........................ 24 Phylogeny of the Quolls ..................... ...................................................................................................................... 25 Genetic Differentiation, Subspeciation, Conservation Units, and the 'Agony of Choice' .......................................................................................................................................................... 27 Genetic Variability........................................................................................................................................................ 32 0 bj ecti ves and Thesis Aims ..... ......... ................ .......... .... .................. ...... .... ................................ ... ....... .... ............. 3 4 References ................ ... ......................... ........ ... ............... ..... ......... .... ... ... ....... .......... ... ... ... ........ ... ......... ... ... ...... ..... ... .. ... ... 3 5 Chapter 2. Isolation and Characterization of Microsatellites from Carnivorous Marsupials (Dasyuridae:Marsupialia) ........................... .. 55 Introduction ..................................................................................................................................................................... 55 Materials and Methods ................................. 55 Results and Discussion .................................... 58 References ................................................................. .. 60 Acknowledgments .......................................... .. 61 v Chapter 3. Phylogenetic Relationships Among Quolls Revisited: the mtDNA Control Region as a Useful Tool .................................................................. 62 Introduction ........... .... .. ...... ........ ................................. ........... ... .......................... .. ...... ... ............ .............. .. ...... ......... .... .. .. 63 Review of Past Phylogenetic Reconstructions of Quolls ....................................... ......... 64 The Control Region as a Phylogenetic Marker ............. .. ... .................................................... 70 Materials and Methods ....... ................ ..... ........... ........... .... ............. ............ ........ ... ..............
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