Improving ecohealth and conservation of Tasmanian devils by characterising microbiomes, viromes and parasite loads

The Tasmanian devil (herein “devil”) is a marsupial that is threatened with extinction by a contagious cancer. To save the species from extinction, the Save the Tasmanian devil program and the Zoo and Aquarium Association established an insurance metapopulation in 2006, breeding and maintaining devils in captivity and using this population as a source for return of animals to the wild. Two primary goals of the insurance metapopulation are 1) to maintain a suite of associated flora and fauna (commensal, symbiotic and parasitic); and 2) to maintain at least 95% of wild-sourced genetic diversity. In this thesis I conducted research that contributes to the goals of the Save the Tasmanian devil program by tackling three separate, but related topics: 1) characterisation of the host virome, 2) compositional changes to the host microbiome following translocation, and 3) the role of genetic diversity on parasite loads. These three studies provide critical information about the health of the devils and inform their conservation. While devil facial tumour disease, the contagious cancer decimating devil populations, has been studied extensively in recent years, other pathogens or diseases affecting devils and their health have been largely overlooked. This is particularly true for viruses. Furthermore, the first step towards conserving host-associated commensal fauna is to identify and characterise it. I contributed to this effort by providing the first comprehensive characterisation of the devil faecal virome. A total of 24 novel marsupial-related RNA and DNA viruses, as well as other known mammalian pathogens were identified. Comparison of the viromes between captive and wild devils showed that captive individuals have significantly lower viral diversity than those in the wild, possibly due to differences in diets and the environment. Preserving commensal microbial diversity, including viruses, while the species is housed in captivity, may provide beneficial functions to the hosts and warrants further research. Through this study, our knowledge of gut-associated viruses in devils has greatly expanded, providing fundamental baseline information that will contribute to the health management and future disease surveillance of this endangered species. Previous studies have shown that captive devils experience microbial diversity loss and have significantly different gut bacterial microbiome compared to their wild counterparts, suggesting signs of dysbiosis. There was concern over the impact microbial diversity loss in captivity may have on devil health, particularly when individuals are returned to the wild. I investigated temporal changes in the devil gut microbiome over the course of two translocations, in which devils were released into the wild. I showed that the gut microbiome of the released animals underwent significant compositional changes, and began to resemble the microbiome of devils native to the release sites, as early as 3 months post-release. This finding suggests that microbiome perturbations previously observed in captivity are not necessarily permanent and that translocated devils can acquire the native/wild microbiome within a short period of time. As such, microbiome perturbations as a result of captivity in devils may not pose a threat as serious as previously thought. This work however, also demonstrates the importance of monitoring the microbiome post-release for assessing the impact of translocation on host microbiome. Devils have very low genetic diversity, including at the major histocompatibility complex (MHC). Individual-level genetic diversity (heterozygosity) has been suggested to play an important role in various fitness-related traits, including parasite load. To understand whether host genetic diversity influences parasite loads in Tasmanian devils, I investigated the relationship between genetic variation at 33 putative neutral and 2 MHC class II-linked microsatellite makers and nematode parasite load in two wild populations of devils. I discovered that reduced MHC class II heterozygosity was associated with increased nematode parasitism, while genome-wide heterozygosity showed no effects. These observations suggest that nematode resistance in the devils is influenced by genetic variation at MHC class II genes (“local effects”), and not a general effect of inbreeding. The findings of this study reiterate the importance of preserving genetic diversity, particularly at functionally important immune genes for optimizing host health, such as improved parasite resistance. Together, the work presented in this thesis explores various health measures relevant to the conservation of Tasmanian devils both in situ and ex situ. Findings from these studies have offered valuable insight into ways we can improve microbiome and genetic management of devils, in line with some of the primary goals of the species’ conservation efforts