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Recently, the koala retrovirus (KoRV) was found to be in the midst of transitioning from exogenous to endogenous form (Stoye 2006; Tarlinton et al. 2006, 2008), enabling study of the process of retroviral endogenization. KoRV is a gammaretrovirus closely related to the gibbon ape leukemia virus (Hanger et al. 2000). The grassland melomys (Melomys burtoni), a rodent native to Australia, has also been found to carry a related retrovirus (Simmons et al. 2011). Analyses of the genomes of humans and other vertebrates suggest that retroviruses have, from a long-term evolutionary perspective, frequently jumped from one species to another and invaded the germ lines of new hosts (Fiebig et al. 2006; Denner 2007; Hayward et al. 2013) and KoRV is likely to be the result of a transspecies transmission.
The geographic distribution of koalas spans the east coast of Australia from northern Queensland to South Australia and historically three subspecies have sometimes been recognized: Phascolarctos cinereus adustus in Queensland, Phascolarctos cinereus cinereus in New South Wales, and Phascolarctos cinereus victor in Victoria and South Australia. The subspecies were designated based on differences in physical features such as body size and fur color, although these differences may be clinal (Lee and Martin 1988; Department of the Environment, Canberra 2014). Analyses of mitochondrial DNA control region sequences have detected different haplotypes between P. c. adustus and the other subspecies, but such differences were not evident between P. c. cinereus and P. c. victor (Houlden et al. 1999). Genetic diversity among southern Australian koalas has been shown to be very low compared with northern populations using both mitochondrial DNA and microsatellite markers (Houlden et al. 1996, 1999).
Koala populations in northern Australia exhibit 100% prevalence of KoRV, with a relatively high average of 165 copies of KoRV per cell, whereas in southern Australian populations many koalas are completely free of the virus (Tarlinton et al. 2006; Simmons et al. 2012). This suggests that KoRV initially affected koalas in northern Australia and is currently spreading to southern populations (Tarlinton et al. 2006, 2008). Using museum specimens of koalas, KoRV was found to be ubiquitous in northern Australian koalas by the late 19th century, with their sequences resembling that of modern KoRV (Avila-Arcos et al. 2013). KoRV has been associated with high rates of leukemia and lymphoma in koalas, and may play a role in susceptibility to Chlamydia infections (Tarlinton et al. 2005, 2008). The process of retroviral endogenization, at least in the case of koalas, may have involved centuries of reduced fitness and susceptibility to disease in the host species (Avila-Arcos et al. 2013). There also appear to be KoRV variants with more limited distributions that are believed to be of more recent origin and possibly exogenous (Shojima, Hoshino, et al. 2013; Shojima, Yoshikawa, et al. 2013; Xu et al. 2013; Shimode et al. 2014).
Each of the 39 enKoRVs examined was shown to be vertically transmitted; each locus was present in the progeny and at least one parent, or in a parent and one or more other koalas known to be kin. Although no novel enKoRVs were detected between the generations, the degree to which additional proliferation of new enKoRVs may continue among koalas is not yet clear. In studies of endogenous murine leukemia viruses (MuLVs), the proliferation of novel ERVs has been examined in highly inbred strains of mice. Novel endogenous proviral integrations into the germ line are very rare in low viremic strains of mice, although they occur more commonly in highly viremic strains (Rowe and Kozak 1980; Herr and Gilbert 1982; Jenkins et al. 1982; Jenkins and Copeland 1985). Yet even in mouse congenic strains in which highly expressed endogenous MuLV loci are bred into a background strain permissive for endogenous MuLV expression (SWR/J), the number of newly acquired proviruses was low (Jenkins and Copeland 1985). In the permissive conditions, only 18.6% of progeny acquired new germ line proviruses with only an average of 0.5 proviruses per individual (Jenkins and Copeland 1985). Although no novel enKoRVs were detected in the koala progeny, the mouse studies suggest that new ERVs may be generated only gradually through transposition or through exogenous KoRV integration.
The low diversity of KoRV may reflect a low mutation rate for enKoRVs in the koala nuclear genome, which should be much slower than the mutation rate of exogenous KoRV retroviruses (Katz and Skalka 1990). The limited polymorphism reported for KoRV among modern and museum archive koalas has suggested that selection among KoRV sequence variants may not have played a strong role in KoRV evolution (Avila-Arcos et al. 2013; Tsangaras et al. 2014). This would not rule out the possibility that enKoRVs may greatly vary in their effects on koala fitness depending on where they integrated in the host genome. It seems likely that selection would favor koalas with fewer enKoRVs, or with enKoRVs that had fewer combined deleterious effects. The overall reduction in fitness of an individual due to enKoRVs would likely depend on the total number of enKoRVs present in the genome (Simmons et al. 2012), on the chromosomal locations of the enKoRVs (Buzdin et al. 2006; Lamprecht et al. 2010), and on whether they had one or two chromosomal copies at enKoRV loci (Bellone et al. 2013).
To identify additional matched flanking sequences on either side of a single proviral locus, all flank sequences were queried against low-coverage koala genomic sequences. For this search, Bowtie2 (version 2.1.0) (Langmead and Salzberg 2012) was run on the Galaxy platform (Giardine et al. 2005; Blankenberg et al. 2010; Goecks et al. 2010). The koala genomic reads had been generated using DNA from Pci-SN404, sequenced on 1/16th of a PTP of the Roche 454 GS FLX+ platform (Roche Applied Science) run at the High-Throughput Sequencing and Genotyping Unit, UIUC, as has been previously described (Ruiz-Rodriguez et al. 2014).
The koala (Phascolarctos cinereus) is a medium-sized, arboreal folivorous marsupial, with a broad but fragmented distribution associated with Eucalyptus spp. woodlands, its primary food source1. The species is listed nationally as vulnerable in response to population declines in the states of Queensland (QLD) and New South Wales (NSW), and the Australian Capital Territory2,3. Despite being overly abundant in the southern extension of their range, koalas in South-East Queensland (SEQLD) are threatened by the population limiting effects of disease4,5 and habitat clearing for urbanization6, which exposes koalas to trauma from vehicle collisions7 and animal attacks8. Despite investments in medical care and species management, there has been a rapid population decline from 1996 through to 2014, with declines of 80% in the Koala Coast and 54% in Pine Rivers in surveyed Queensland populations9,10.
A recent retrospective epidemiological study using passive surveillance hospital records of koala mortality spanning 17 years determined several major factors drive koala hospital submissions. Vehicle collisions, and chlamydiosis-associated debilitation and infertility were the major causes of mortality and morbidity10,11. However, this study was based on retrospective medical records and necropsies were not conducted in all animals, impeding the detailed interrogation of comorbidity and disease interaction10. Given the complex threats affecting the koala population and the high prevalence of disease and injury found in this retrospective study, a passive surveillance necropsy study was undertaken.
Passive surveillance utilizes medical records or data produced by other health-related activities12, and is an increasingly popular method for wildlife studies due to its cost-effectiveness and the feasibility of collecting information across multiple seasons. In this study, a passive surveillance method was used to recruit koalas for detailed necropsy examination. The purpose of this prospective pathology study was to apply systematic necropsy and data recording methodology to accurately identify causes of mortality and to interrogate the interplay of comorbidities driving terminal koala submissions to hospitals in SEQLD. This is the one of the most extensive pathological studies applied to a declining wild species in Australia, identifying major causes of death, comorbidity trends and permitting the statistical evaluation of variables influencing threats to the species.
Percentage of koalas by body condition category with co-morbidities absent or present (N = 519). Koalas were submitted to South-East Queensland hospitals and receiving necropsies at The University of Queensland from 2013 through to 2016.
Renal complications compatible with chlamydial infection affected 34.8% (106/304) of all koalas and included 9/106 cases of hydronephrosis (Fig. 3c) and 13/106 of renal pyramidal fibrosis from chronic chlamydial pyelonephritis (Fig. 3d). Primary renal disease was also observed without cystitis in 51.8% (43/83) cases. The predominant histological lesion was lymphocytic interstitial nephritis or chronic lymphocytic segmental pyelonephritis. Severe renal disease was infrequent, and included ascending urinary tract infection - UTI (4 cases), end stage kidney disease (4 cases), and pyelonephritis (10 cases). Renal crystal precipitation was observed in 21 cases, mostly morphologically consistent with struvite in 47.6% (10/21) cases, and calcium oxalate in 23.8% cases (5/21). 2b1af7f3a8