Emergence, transmission and evolution of an uncommon enemy: Tasmanian devil facial tumour disease

The Tasmanian devil ( Sarcophilus harrisii ) is at risk of extinction owing to the emergence of a contagious cancer known as devil facial tumour disease (DFTD). The emergence and spread of DFTD has been linked to low genetic diversity in the major histocompatibility complex (MHC). We examined MHC diversity in historical and ancient devils to determine whether loss of diversity is recent or predates European settlement in Australia. Our results reveal no additional diversity in historical Tasmanian samples. Mainland devils had common modern variants plus six new variants that are highly similar to existing alleles. We conclude that low MHC diversity has been a feature of devil populations since at least the Mid-Holocene and could explain their tumultuous history of population crashes.

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The effects of season and devil facial tumour disease on the reproductive physiology of the male Tasmanian devil (Sarcophilus harrisii)

Reproduction Fertility and Development ◽

10.1071/rd11134 ◽

2012 ◽

Vol 24 (7) ◽

pp. 999 ◽

Cited By ~ 7

Author(s):

T. Keeley ◽

P. D. McGreevy ◽

J. K. O'Brien

Keyword(s):

Early Stage ◽

Reproductive Function ◽

Serum Testosterone ◽

Serum Cortisol ◽

Disease Stage ◽

Rapid Decline ◽

Tasmanian Devil ◽

Early Stage Disease ◽

Devil Facial Tumour Disease ◽

Disease Free

Devil facial tumour disease (DFTD) is the cause of the rapid decline of wild Tasmanian devils. Female devils are seasonal breeders with births peaking during autumn (i.e. March) but the degree of reproductive seasonality in male devils is unknown. The objective of this study was to examine the potential effects of season and DFTD on reproductive function in male devils (n = 55). Testicular (1.90 ± 0.23 g) and epididymal (0.90 ± 0.06 g) weights were maximal during autumn and spring (P < 0.05), whereas prostate (3.71 ± 0.74 g) and Cowper’s gland (0.68 ± 0.22; 0.52 ± 0.21 g) weights peaked during autumn (P < 0.001). The motility of spermatozoa from the cauda epididymides extracted post-mortem was similar (P > 0.05) across season and disease state (31.5 ± 13.1% total motility). Testicular and epididymal weights were no different between animals displaying late or early-stage DTFD signs or disease-free animals (P > 0.1). The accessory sex glands were larger in late-stage DFTD animals than in animals with early-stage disease signs or which were disease-free (P < 0.01) but effects of season on this result can’t be excluded. Serum testosterone concentrations peaked during summer (0.25 ± 0.18 ng mL–1) but values were not different from the preceding and subsequent seasons (P > 0.05), nor influenced by disease stage (P > 0.1). Seasonal and DFTD-related changes in serum cortisol concentrations were not evident (P > 0.1). Male devil reproduction does not appear to be restricted by season nor inhibited by DFTD.

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Marsupial chromosomics: bridging the gap between genomes and chromosomes

Reproduction Fertility and Development ◽

10.1071/rd18201 ◽

2019 ◽

Vol 31 (7) ◽

pp. 1189 ◽

Cited By ~ 1

Author(s):

Janine E. Deakin ◽

Sally Potter

Keyword(s):

Dna Sequence ◽

Genome Assembly ◽

Genome Architecture ◽

Sequence Information ◽

Full Potential ◽

Tasmanian Devil ◽

Sequencing Technology ◽

A Genome ◽

Devil Facial Tumour Disease ◽

Chromosome Level

Marsupials have unique features that make them particularly interesting to study, and sequencing of marsupial genomes is helping to understand their evolution. A decade ago, it was a huge feat to sequence the first marsupial genome. Now, the advances in sequencing technology have made the sequencing of many more marsupial genomes possible. However, the DNA sequence is only one component of the structures it is packaged into: chromosomes. Knowing the arrangement of the DNA sequence on each chromosome is essential for a genome assembly to be used to its full potential. The importance of combining sequence information with cytogenetics has previously been demonstrated for rapidly evolving regions of the genome, such as the sex chromosomes, as well as for reconstructing the ancestral marsupial karyotype and understanding the chromosome rearrangements involved in the Tasmanian devil facial tumour disease. Despite the recent advances in sequencing technology assisting in genome assembly, physical anchoring of the sequence to chromosomes is required to achieve a chromosome-level assembly. Once chromosome-level assemblies are achieved for more marsupials, we will be able to investigate changes in the packaging and interactions between chromosomes to gain an understanding of the role genome architecture has played during marsupial evolution.

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DYNAMICAL SYSTEMS ANALYSIS OF A MODEL DESCRIBING TASMANIAN DEVIL FACIAL TUMOUR DISEASE

The ANZIAM Journal ◽

10.1017/s1446181113000011 ◽

2012 ◽

Vol 54 (1-2) ◽

pp. 89-107 ◽

Cited By ~ 4

Author(s):

N. J. BEETON ◽

L. K. FORBES

Keyword(s):

Dynamical Systems ◽

Systems Analysis ◽

Small Amplitude ◽

Systems Approach ◽

Steady States ◽

Tasmanian Devil ◽

Bifurcation Parameter ◽

Disease Dynamics ◽

Dynamical Systems Analysis ◽

Devil Facial Tumour Disease

AbstractA susceptible–exposed–infectious theoretical model describing Tasmanian devil population and disease dynamics is presented and mathematically analysed using a dynamical systems approach to determine its behaviour under a range of scenarios. The steady states of the system are calculated and their stability analysed. Closed forms for the bifurcation points between these steady states are found using the rate of removal of infected individuals as a bifurcation parameter. A small-amplitude Hopf region, in which the populations oscillate in time, is shown to be present and subjected to numerical analysis. The model is then studied in detail in relation to an unfolding parameter which describes the disease latent period. The model’s behaviour is found to be biologically reasonable for Tasmanian devils and potentially applicable to other species.

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Relict or reintroduction? Genetic population assignment of three Tasmanian devils ( Sarcophilus harrisii ) recovered on mainland Australia

Royal Society Open Science ◽

10.1098/rsos.170053 ◽

2017 ◽

Vol 4 (4) ◽

pp. 170053 ◽

Cited By ~ 1

Author(s):

Lauren C. White ◽

Jeremy J. Austin

Keyword(s):

Tasmanian Devil ◽

Nucleotide Polymorphisms ◽

Genetic Population ◽

Single Nucleotide ◽

Mainland Population ◽

Devil Facial Tumour Disease ◽

Eastern Australia ◽

The Devil ◽

Disease Free ◽

Sarcophilus Harrisii

Today, the Tasmanian devil ( Sarcophilus harrisii ) is found only on the island of Tasmania, despite once being widespread across mainland Australia. While the devil is thought to have become extinct on the mainland approximately 3000 years ago, three specimens were collected in Victoria (south-eastern Australia) between 1912 and 1991, raising the possibility that a relict mainland population survived in the area. Alternatively, these devils may have escaped captivity or were deliberately released after being transported from Tasmania, a practice that has been strictly controlled since the onset of devil facial tumour disease in the early 1990s. Such quarantine regimes are important to protect disease-free, ‘insurance populations’ in zoos on the mainland. To test whether the three Victorian devils were members of a relict mainland population or had been recently transported from Tasmania we identified seven single nucleotide polymorphisms (SNPs) in the mitochondrial genome that can distinguish between Tasmanian and ancient mainland populations. The three Victorian devil specimens have the same seven SNPs diagnostic of modern Tasmanian devils, confirming that they were most likely transported from Tasmania and do not represent a remnant population of mainland devils.

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Are any populations 'safe'? Unexpected reproductive decline in a population of Tasmanian devils free of devil facial tumour disease

Wildlife Research ◽

10.1071/wr16234 ◽

2018 ◽

Vol 45 (1) ◽

pp. 31 ◽

Cited By ~ 7

Author(s):

K. A. Farquharson ◽

R. M. Gooley ◽

S. Fox ◽

S. J. Huxtable ◽

K. Belov ◽

...

Keyword(s):

Conservation Management ◽

Southern Oscillation ◽

Demographic Data ◽

Management Strategies ◽

Natural Populations ◽

Significant Decline ◽

Tasmanian Devil ◽

Devil Facial Tumour Disease ◽

In The Wild ◽

Reproductive Rates

Context Conservation management relies on baseline demographic data of natural populations. For Tasmanian devils (Sarcophilus harrisii), threatened in the wild by two fatal and transmissible cancers (devil facial tumour disease DFTD: DFT1 and DFT2), understanding the characteristics of healthy populations is crucial for developing adaptive management strategies to bolster populations in the wild. Aims Our analysis aims to evaluate contemporary reproductive rates for wild, DFTD-free Tasmanian devil populations, and to provide a baseline with which to compare the outcome of current translocation activities. Methods We analysed 8 years of field-trapping data, including demographics and reproductive rates, across 2004–16, from the largest known DFTD-free remnant population at Woolnorth, Tasmania. Key results Surprisingly, we found a dramatic and statistically significant decline in female breeding rate when comparing data collected from 2004–2009 with data from 2014–2016. Unfortunately we do not have any data from the intermediate years. This decline in breeding rate was accompanied by a subtle but statistically significant decline in litter sizes. These changes were not associated with a change in body condition over the same period. Furthermore, we could not attribute the decline in breeding to a change in population size or sex ratio. Preliminary analysis suggested a possible association between annual breeding rate and coarse measures of environmental variation (Southern Oscillation Index), but any mechanistic associations are yet to be determined. Conclusions The decline in breeding rates was unexpected, so further monitoring and investigation into potential environmental and/or biological reasons for the decline in breeding rate are recommended before the arrival of DFTD at Woolnorth. Implications Our results provide valuable data to support the conservation management of Tasmanian devils in their native range. They also highlight the importance of continued monitoring of ‘safe’ populations, in the face of significant threats elsewhere.

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Efficiently locating conservation boundaries: Searching for the Tasmanian devil facial tumour disease front

Biological Conservation ◽

10.1016/j.biocon.2009.01.029 ◽

2009 ◽

Vol 142 (7) ◽

pp. 1333-1339 ◽

Cited By ~ 7

Author(s):

Michael Bode ◽

Clare Hawkins ◽

Tracy Rout ◽

Brendan Wintle

Keyword(s):

Tasmanian Devil ◽

Devil Facial Tumour Disease

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Cathelicidin-3 associated with serum extracellular vesicles enables early diagnosis of a transmissible cancer

10.1101/2021.12.06.471373 ◽

2021 ◽

Author(s):

Camila Espejo ◽

Richard Wilson ◽

Ruth J. Pye ◽

Julian C. Ratcliffe ◽

Manuel Ruiz-Aravena ◽

...

Keyword(s):

Early Diagnosis ◽

Biomarker Discovery ◽

Extracellular Vesicle ◽

Conservation Strategies ◽

Tasmanian Devil ◽

Serum Samples ◽

Visual Identification ◽

Devil Facial Tumour Disease ◽

Transmissible Cancer ◽

One Year

AbstractThe identification of practical early diagnosis biomarkers is a cornerstone of improved prevention and treatment of cancers. Such a case is devil facial tumour disease (DFTD), a highly lethal transmissible cancer afflicting virtually an entire species, the Tasmanian devil (Sarcophilus harrisii). Despite a latent period that can exceed one year, to date DFTD diagnosis requires visual identification of tumour lesions. To enable earlier diagnosis, which is essential for the implementation of effective conservation strategies, we analysed the extracellular vesicle (EV) proteome of 87 Tasmanian devil serum samples. The antimicrobial peptide cathelicidin-3 (CATH3) was enriched in serum EVs of both devils with clinical DFTD (87.9% sensitivity and 94.1% specificity) and devils with latent infection (i.e., collected while overtly healthy, but 3-6 months before subsequent DFTD diagnosis; 93.8% sensitivity and 94.1% specificity). As antimicrobial peptides can play a variety of roles in the cancer process, our results suggest that the specific elevation of serum EV-associated CATH3 may be mechanistically involved in DFTD pathogenesis. This EV-based approach to biomarker discovery is directly applicable to improving understanding and diagnosis of a broad range of diseases in other species, and these findings directly enhance the capacity of conservation strategies to ensure the viability of the imperilled Tasmanian devil population.

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