Introduction
Disease can pose a serious threat to flora and fauna, recently demonstrated through the global impact of white nose syndrome , sarcoptic mange , and anthrax . Similarly, plant diseases such as chestnut blight and Dutch elm disease have had large-scale impacts on species and ecosystem diversity . It is also likely that threats to wildlife populations from disease will increase in frequency, due to interactions with both climate change and accelerating anthropogenic disturbances . In addition to the threat to biodiversity, wildlife diseases can have substantial economic impacts and affect ecosystem services . Wildlife diseases also pose a growing threat to human health, with an estimated 75% of emerging infectious diseases in humans being of wildlife origin (Merianos 2007).
Managing diseases in wild populations is difficult, in part because effective management of disease requires an understanding of host-pathogen-environment dynamics that may be costly to obtain . Intensive management such as vaccination might only be feasible in certain situations, where vaccines can be distributed in baits that are readily taken (e.g. rabies vaccine for carnivores, ) or for small, contained populations . Targeted disease mitigation strategies in the case of the chytrid fungus in amphibians, for instance, have included preventing pathogen spread to naive populations, establishing ex-situ insurance colonies, and captive breeding of amphibian hosts . To achieve effective management of already-infected populations, however, mitigation strategies need to integrate specific host-pathogen interactions, in particular targeting pathogenicity and host susceptibility . Moreover, as part of the increased appreciation of the value of evolutionary insights for wildlife disease management, there is increasing awareness of the need to understand what factors contribute to susceptibility to disease. This information can be fundamental in predicting whether species and populations will adapt to diseases, and could enable us to assist this process by selecting resilient animals .
Many factors influence the susceptibility of a host to a pathogen. The host’s environment will have multiple effects on its susceptibility to disease: for example, the quality and quantity of food resources can influence host condition and hence immunological health , and both the prevalence of the pathogen and characteristics of individuals’ social environment can affect infection risk . Host genetics may also play a role in determining individuals’ suceptibility to disease . For example, genetic variation may affect susceptibility via additive genetic effects (Hill 2012). Another genetic characteristic related to the ability of a host to cope with disease is inbreeding, the risk of which increases with small populations. Links between inbreeding and lowered disease resilience (i.e., the cumulative impact of resistance and tolerance) may be driven by inbreeding depression, explained through decreased heterozygosity in genes of the immune system (e.g., major histo-compatibility complex ), and the loss of alleles linked to resilience . As such, determining the extent of heritability of susceptibility to disease and potential inbreeding depression linked to the disease could be valuable for disease management. In particular, a genetically heritable basis to variation in susceptibility indicates the potential for evolutionary responses, and for selective breeding for resistance, whereas the existence of strong effects of inbreeding would support efforts to improve genetic variance within populations.
In this study, we present quantitative genetic and inbreeding analyses of a disease affecting an Australian mammal, the koalaPhascolarctos cinereus . Recent declines in population size, including those due to extreme bushfires in 2020, have led to the classification of koalas in Queensland, New South Wales, and the Australian Capital Territory (approximately 60% of their range) as endangered in 2022. Whilst the bushfires decimated large areas of koala habitat, the bacterial pathogen Chlamydia has been identified as a major threat to their survival . The bacterium causes chlamydial disease, which primarily affects the ocular and urogenital tracts in koalas and decreases both survival and reproduction rates . The main transmission path is sexual, although some mother-offspring transmission does occur . The severity of chlamydial disease varies greatly both between and within populations , and not all koalas that are infected progress to ‘diseased’ status (i.e., show clinical signs of disease) . Chlamydial disease is the most common illness causing death of wild koalas and is such a critical threat to koalas that, when adequately addressed, population declines can be reversed . However, management of the disease currently requires costly treatment, including catching koalas and multiple weeks of antibiotic treatment at wildlife hospitals . An understanding of the potential for evolutionary responses could therefore greatly improve management strategies for koala populations.
Using high-resolution data from a wild population of koalas, we investigated the effect of genetic and environmental factors on chlamydia disease. There is a high prevalence of chlamydia disease in the study population (28%, ), and chlamydia is a leading cause of mortality (18% of all deaths, ). Further, we have previously demonstrated that koalas in this population do not avoid mating with either diseased, or with closely-related individuals . Here we aimed to 1) determine whether there was evidence for inbreeding depression associated with disease susceptibility of koalas, and 2) partition variance in koalas’ susceptibility to disease into additive genetic and environmental components. Our analysis provides insight into the extent to which an individual’s genes and/or environment affects their susceptibility to disease, and whether a wild population could respond to selection for improved resilience to chlamydial disease.