Conservation genetics of the koala (Phascolarctos cinereus) in Queensland and Northeast New South Wales

The koala (Phascolarctos cinereus) is an iconic Australian marsupial that is the sole extant representative of the Family Phascolarctidae and forms part of the mammalian fauna in four Australian States and one Territory. There has been a significant decline in the range and distribution of the koala since European settlement, with habitat loss and its associated threats, including vehicle strikes, dog attacks and disease, continuing to reduce population numbers. Koalas provide the tourism industry and the Australian economy with revenue up to $1 billion per annum with 80 zoos and wildlife parks around the country displaying koalas. Koalas were introduced to a number of islands in southern Australia the early 20th century, in an attempt to ‘save’ them from near extinction due to habitat loss, hunting and disease. While populations on Queensland islands remain stable and require no management intervention, introduced populations on southern Australian islands show extremely low levels of genetic diversity yet have grown substantially and require constant monitoring and management to overcome overabundance and starvation associated with defoliation of food trees. The only known extant, naturally occurring, island population of koalas is on North Stradbroke Island in Southeast Queensland’s Moreton Bay. Infection with bacteria of the Family Chlamydiacae is at high prevalence in most koala populations but the resulting diseases are generally of low prevalence in koalas in Southeast Queensland and New South Wales. The role of the koala retrovirus (KoRV) in relation to infectious diseases is not fully understood, but it has been identified from all northern koala populations and the majority of southern koala populations though, like chlamydial infection, it is not usually associated with high disease prevalence. The major histocompatability complex (MHC) is a gene family in mammals that is vital for its role in disease resistance and so may play a role in disease susceptibility in koalas. This study provided detailed information about the genetic diversity and population structuring of the mainland koala population in Southeast Queensland, which is amongst the most threatened of koala populations because of anthropogenic disturbance. Microsatellite genotyping of 512 samples and mitochondrial DNA sequencing of a subset of 77 samples collected from sick, injured and dead koalas showed that in Southeast Queensland koalas had high microsatellite diversity (12.8 alleles/locus, He = 0.81) and at least 16 mitochondrial haplotypes. Population genetic analysis revealed six genetically differentiated clusters consistent with the existence of biogeographic and anthropogenic barriers like rivers and highways. The Koala Coast, an area in Southeast Queensland that provides habitat for one of the most significant natural koala populations in Australia was found to be genetically distinct from adjacent areas; the rapid decline of this population means it meets the criteria for classification as “Endangered Wildlife” under Queensland’s Nature Conservation Act 1992. Climatic patterns of warming and cooling that produced the disappearance and reappearance of rainforests is likely to have affected long term koala distribution in coastal eastern Australia – expansion into drier forests when they were available and restriction to refugia during times of rainforest dominance. The koala population in Northeast New South Wales, which has conventionally been classified as a different subspecies to the koalas in Southeast Queensland, has colonised an extensive part of the area since the destruction of the “Big Scrub” rainforest. This forest occupied about 75,000 ha before European settlement and would almost certainly have represented a natural barrier to the movement of koalas as it was unsuitable habitat due to its lack of suitable food trees. Population structuring analysis identified two major genetic clusters in the region, the northernmost of which was less differentiated from koalas sampled on the Gold Coast in Southeast Queensland than the southernmost cluster. The southern cluster, largely found around the city of Lismore, had significantly lower diversity than the northern cluster, consistent with a southward radiating colonisation pathway. Ninety-six percent (96%) of koalas in Northeast New South Wales shared the same mitochondrial DNA haplotype, which was the most common haplotype in Southeast Queensland. There was, therefore, little evidence to support the subspecies delineation of coastal koalas in Southeast Queensland and Northeast New South Wales. From a comparison between wild, mainland populations and two captive koala colonies in Southeast Queensland, genetic diversity in 106 captive koalas was found to be similar to the local wild populations (Dreamworld 9.2 alleles/locus, He = 0.75, Currumbin Wildlife Sanctuary 10.2 alleles/locus, He = 0.80). Microsatellite alleles in captive koalas were, in general, representative of the local wild populations and of similar frequencies, but the captive koalas possessed mitochondrial DNA haplotypes that were not found in the local wild koalas. Some of the original founders of the captive populations were not from Southeast Queensland so these different mitochondrial haplotypes are likely remnants of the koala genotypes at the original founders’ locations. The preservation of habitat and reduction of consequential threats to the koala’s long term survival in the wild are the most fundamental aspects of koala conservation in this region. However, the successful preservation of high genetic diversity at neutral loci in the captive colonies studied indicates that ex situ measures incorporating a captive breeding program could potentially be used as reservoirs for important genetic material should such an approach become necessary in the context of the drastic and accelerating decline towards local extinction of key Southeast Queensland koala populations. Urgent action would be essential to obtain a representative sample of current genetic diversity (both genomic and mitochondrial), given the drastic rate of decline. Island populations of organisms are expected to show reduced genetic diversity compared to their mainland counterparts because of factors such as founder effects and the increased susceptibility of small populations to the effects of genetic drift. A comparison of genetic diversity was made between the naturally occurring North Stradbroke Island koala population in Southeast Queensland and the introduced populations on St Bees, Brampton, Newry and Rabbit Islands in central Queensland with the mainland populations. As expected, the island populations had lower genetic diversity than mainland populations, however, the introduced St Bees Island population had higher mean number of alleles and expected heterozygosity (5.7 alleles/locus, He = 0.67) than the naturally occurring population on North Stradbroke Island (3.7 alleles/locus, He = 0.55). Anecdotal evidence suggests that the koala populations on Brampton, Newry and Rabbit Islands off the central Queensland coast were established by the unauthorised transfer of koalas from St Bees Island. Mitochondrial DNA haplotype analysis supports this claim however, the most likely explanations for the presence of at least four microsatellite alleles in the Brampton, Newry and Rabbit Island populations that were not found in St Bees Island koalas are that either there were additional introductions from elsewhere or that koalas were already present on these islands prior to the transfers from St Bees Island. A study on the prevalence of chlamydial and retroviral infection in captive and wild koalas showed that 100% of koalas in this study had retroviral and chlamydial infection in at least one tested swab site. None of the captive animals showed clinical signs of disease despite the high prevalence of infection. Signs of disease were evident in some wild koalas, which, in some cases, was the reason for their admission to Moggill Koala Hospital for treatment. In an attempt to understand the immunological mechanisms underlying the apparent disease resistance of koalas which usually limits latent infection progressing to clinical disease states, the MHC genes of koalas were investigated. Low variation at MHC loci is thought to increase susceptibility to infectious diseases because fewer foreign antigens are recognised. The first class II sequences identified from koalas are presented here and showed variation. Variation was also detected at exon 3 of class I, with evidence for at least three class I loci. The koala is a unique Australian marsupial that makes a nationally significant contribution to the Australian economy annually. The results of this study have important conservation and management implications for koala populations in Southeast Queensland and Northeast New South Wales - particularly declining populations in Southeast Queensland - as well as being informative on other aspects of the species’ biology and for mammalian conservation genetics, generally.

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