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.