A Tasmanian devil breeding program to support wild recovery

Tasmanian devils are threatened in the wild by devil facial tumour disease: a transmissible cancer with a high fatality rate. In response, the Save the Tasmanian Devil Program (STDP) established an ‘insurance population’ to enable the preservation of genetic diversity and natural behaviours of devils. This breeding program includes a range of institutions and facilities, from zoo-based intensive enclosures to larger, more natural environments, and a strategic approach has been required to capture and maintain genetic diversity, natural behaviours and to ensure reproductive success. Laboratory-based research, particularly genetics, in tandem with adaptive management has helped the STDP reach its goals, and has directly contributed to the conservation of the species in the wild. Here we review this work and show that the Tasmanian devil breeding program is a powerful example of how genetic research can be used to understand and improve reproductive success in a threatened species.

Download Full-text

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.

Download Full-text

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.

Download Full-text

Disruption of Metapopulation Structure Reduces Tasmanian Devil Facial Tumour Disease Spread at the Expense of Abundance and Genetic Diversity

Pathogens ◽

10.3390/pathogens10121592 ◽

2021 ◽

Vol 10 (12) ◽

pp. 1592

Author(s):

Rowan Durrant ◽

Rodrigo Hamede ◽

Konstans Wells ◽

Miguel Lurgi

Keyword(s):

Genetic Diversity ◽

Disease Transmission ◽

Transmission Rate ◽

Extinction Risk ◽

Disease Prevalence ◽

Disease Spread ◽

Tasmanian Devil ◽

Local Populations ◽

Metapopulation Structure ◽

Devil Facial Tumour Disease

Metapopulation structure plays a fundamental role in the persistence of wildlife populations. It can also drive the spread of infectious diseases and transmissible cancers such as the Tasmanian devil facial tumour disease (DFTD). While disrupting this structure can reduce disease spread, it can also impair host resilience by disrupting gene flow and colonisation dynamics. Using an individual-based metapopulation model we investigated the synergistic effects of host dispersal, disease transmission rate and inter-individual contact distance for transmission, on the spread and persistence of DFTD from local to regional scales. Disease spread, and the ensuing population declines, are synergistically determined by individuals’ dispersal, disease transmission rate and within-population mixing. Transmission rates can be magnified by high dispersal and inter-individual transmission distance. The isolation of local populations effectively reduced metapopulation-level disease prevalence but caused severe declines in metapopulation size and genetic diversity. The relative position of managed (i.e., isolated) local populations had a significant effect on disease prevalence, highlighting the importance of considering metapopulation structure when implementing metapopulation-scale disease control measures. Our findings suggest that population isolation is not an ideal management method for preventing disease spread in species inhabiting already fragmented landscapes, where genetic diversity and extinction risk are already a concern.

Download Full-text

Blood Parasites in Endangered Wildlife-Trypanosomes Discovered during a Survey of Haemoprotozoa from the Tasmanian Devil

Pathogens ◽

10.3390/pathogens9110873 ◽

2020 ◽

Vol 9 (11) ◽

pp. 873

Author(s):

Siobhon L. Egan ◽

Manuel Ruiz-Aravena ◽

Jill M. Austen ◽

Xavier Barton ◽

Sebastien Comte ◽

...

Keyword(s):

Emerging Infectious Diseases ◽

Protozoan Parasite ◽

Blood Parasites ◽

Rapid Decline ◽

Tasmanian Devil ◽

Devil Facial Tumour Disease ◽

Transmissible Cancer ◽

Carnivorous Marsupial ◽

The Impact ◽

Single Blood Sample

The impact of emerging infectious diseases is increasingly recognised as a major threat to wildlife. Wild populations of the endangered Tasmanian devil, Sarcophilus harrisii, are experiencing devastating losses from a novel transmissible cancer, devil facial tumour disease (DFTD); however, despite the rapid decline of this species, there is currently no information on the presence of haemoprotozoan parasites. In the present study, 95 Tasmanian devil blood samples were collected from four populations in Tasmania, Australia, which underwent molecular screening to detect four major groups of haemoprotozoa: (i) trypanosomes, (ii) piroplasms, (iii) Hepatozoon, and (iv) haemosporidia. Sequence results revealed Trypanosoma infections in 32/95 individuals. Trypanosoma copemani was identified in 10 Tasmanian devils from three sites and a second Trypanosoma sp. was identified in 22 individuals that were grouped within the poorly described T. cyclops clade. A single blood sample was positive for Babesia sp., which most closely matched Babesia lohae. No other blood protozoan parasite DNA was detected. This study provides the first insight into haemoprotozoa from the Tasmanian devil and the first identification of Trypanosoma and Babesia in this carnivorous marsupial.

Download Full-text

Sex bias in ability to cope with cancer: Tasmanian devils and facial tumour disease

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2018.2239 ◽

2018 ◽

Vol 285 (1891) ◽

pp. 20182239 ◽

Cited By ~ 14

Author(s):

Manuel Ruiz-Aravena ◽

Menna E. Jones ◽

Scott Carver ◽

Sergio Estay ◽

Camila Espejo ◽

...

Keyword(s):

Cancer Progression ◽

Body Condition ◽

Interspecific Interactions ◽

Reaction Norm ◽

Life History Strategies ◽

Tasmanian Devil ◽

Devil Facial Tumour Disease ◽

Transmissible Cancer ◽

The Individual ◽

Host Tolerance

Knowledge of the ecological dynamics between hosts and pathogens during the initial stages of disease emergence is crucial to understanding the potential for evolution of new interspecific interactions. Tasmanian devil ( Sarcophilus harrisii ) populations have declined precipitously owing to infection by a transmissible cancer (devil facial tumour disease, DFTD) that emerged approximately 20 years ago. Since the emergence of DFTD, and as the disease spreads across Tasmania, the number of devils has dropped up to 90% across 80% of the species's distributional range. As a result, the disease is expected to act as a strong selective force on hosts to develop mechanisms of tolerance and/or resistance to the infection. We assessed the ability of infected devils to cope with infection, which translates into host tolerance to the cancer, by using the reaction norm of the individual body condition by tumour burden. We found that body condition of infected hosts is negatively affected by cancer progression. Males and females presented significant differences in their tolerance levels to infection, with males suffering declines of up to 25% of their body condition, in contrast to less than 5% in females. Sex-related differences in tolerance to cancer progression may select for changes in life-history strategies of the host and could also alter the selective environment for the tumours.

Download Full-text

Multiple paternity and precocial breeding in wild Tasmanian devils, Sarcophilus harrisii (Marsupialia: Dasyuridae)

Biological Journal of the Linnean Society ◽

10.1093/biolinnean/blz072 ◽

2019 ◽

Vol 128 (1) ◽

pp. 201-210 ◽

Cited By ~ 1

Author(s):

Tracey Russell ◽

Amanda Lane ◽

Judy Clarke ◽

Carolyn Hogg ◽

Katrina Morris ◽

...

Keyword(s):

Genetic Diversity ◽

Multiple Paternity ◽

First Record ◽

Good Genes ◽

Tasmanian Devil ◽

Histocompatibility Complex ◽

Insurance Programme ◽

In The Wild ◽

Marsupial Species ◽

Sarcophilus Harrisii

Abstract Polyandry, a common reproductive strategy in various animal species, has potential female benefits, which include enhanced offspring fitness. Benefits can be direct, such as reduced risk of male infanticide of offspring, or indirect, such as increased genetic diversity of offspring and the acquisition of ‘good genes’. Multiple paternity of litters has been recorded in numerous marsupial species but has not been reported in Tasmanian devils, Sarcophilus harrisii (Boitard). We investigated whether multiple paternity occurred in litters within a wild population of Tasmanian devils. Using major histocompatibility complex-linked and neutral microsatellite markers, the paternity of nine litters was analysed. We found multiple paternity in four out of nine litters and that yearling (> 1, < 2 years old) male devils were siring offspring. This is the first record of multiple paternity and of male precocial breeding in wild Tasmanian devils. To date, there are no data relating to the subsequent survival of devils from single- vs. multiple-sired litters; therefore, we do not know whether multiple paternity increases offspring survival in the wild. These results have implications for the Tasmanian devil captive insurance programme, because group housing can lead to multiple-sired litters, making the maintenance of genetic diversity over time difficult to manage.

Download Full-text

Ethyl-Iophenoxic acid as a serum marker for oral baiting of carnivorous marsupials

10.1101/2021.12.14.472710 ◽

2021 ◽

Author(s):

Ruth Pye ◽

David S Nichols ◽

Amy T. Gilbert ◽

Andrew S Flies

Keyword(s):

Field Trials ◽

Serum Marker ◽

Negative Control ◽

Vaccine Uptake ◽

Tasmanian Devil ◽

Serum Samples ◽

Baseline Serum ◽

Wildlife Species ◽

Devil Facial Tumour Disease ◽

In The Wild

Context: Ethyl-Iophenoxic acid (Et-IPA) has been widely used as a bait biomarker to determine oral bait consumption by vertebrate wildlife species. Oral bait vaccines have been delivered to numerous wildlife species to protect them from disease. The Tasmanian devil (Sarcophilis harrisii), the largest extant carnivorous marsupial species, is threatened by the transmissible cancers known as devil facial tumour disease (DFTD). Development of a protective DFTD vaccine is underway, and an oral bait has been proposed to deliver the vaccine in the wild. The bait delivery system requires a biomarker that can be detected for several months post-consumption in Tasmanian devils. Aim: To determine the suitability of Et-IPA as a bait biomarker in the Tasmanian devil. Method: Two Tasmanian devils were fed 50 mg Et-IPA (4.5 to 7.1 mg Et-IPA/kg bodyweight). Liquid chromatography with tandem mass spectrometry (LC-MS/-MS) was used to directly measure Et-IPA in baseline serum samples and samples collected on days 1, 14, 26 and 56 post-baiting. Key results: Both devils retained serum Et-IPA concentrations at two orders of magnitude above negative control sera when this study concluded. Conclusions: Et-IPA is a useful bait biomarker for Tasmanian devils and can be included in future DFTD bait vaccine field trials to determine bait vaccine uptake.

Download Full-text

Transmissible cancer in Tasmanian devils: localized lineage replacement and host population response

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.1468 ◽

2015 ◽

Vol 282 (1814) ◽

pp. 20151468 ◽

Cited By ~ 32

Author(s):

Rodrigo K. Hamede ◽

Anne-Maree Pearse ◽

Kate Swift ◽

Leon A. Barmuta ◽

Elizabeth P. Murchison ◽

...

Keyword(s):

Population Decline ◽

Emerging Infectious Diseases ◽

Infectious Agent ◽

Host Population ◽

Future Research ◽

Tasmanian Devil ◽

Genetic Management ◽

Genetic Lineages ◽

Devil Facial Tumour Disease ◽

Transmissible Cancer

Tasmanian devil facial tumour disease (DFTD) is a clonally transmissible cancer threatening the Tasmanian devil ( Sarcophilus harrisii ) with extinction. Live cancer cells are the infectious agent, transmitted to new hosts when individuals bite each other. Over the 18 years since DFTD was first observed, distinct genetic and karyotypic sublineages have evolved. In this longitudinal study, we investigate the associations between tumour karyotype, epidemic patterns and host demographic response to the disease. Reduced host population effects and low DFTD infection rates were associated with high prevalence of tetraploid tumours. Subsequent replacement by a diploid variant of DFTD coincided with a rapid increase in disease prevalence, population decline and reduced mean age of the population. Our results suggest a role for tumour genetics in DFTD transmission dynamics and epidemic outcome. Future research, for this and other highly pathogenic emerging infectious diseases, should focus on understanding the evolution of host and pathogen genotypes, their effects on susceptibility and tolerance to infection, and their implications for designing novel genetic management strategies. This study provides evidence for a rapid localized lineage replacement occurring within a transmissible cancer epidemic and highlights the possibility that distinct DFTD genetic lineages may harbour traits that influence pathogen fitness.

Download Full-text

Genetic diversity, phylogenetic relationships and conservation of Edwards's Pheasant Lophura edwardsi

Bird Conservation International ◽

10.1017/s095927090000215x ◽

1998 ◽

Vol 8 (4) ◽

pp. 395-410 ◽

Cited By ~ 1

Author(s):

Alain Hennache ◽

Ettore Randi ◽

Vittorio Lucchini

Keyword(s):

Genetic Diversity ◽

Captive Breeding ◽

Nuclear Dna ◽

Genetic Research ◽

Ex Situ ◽

Historical Study ◽

Evolutionary Divergence ◽

Taxonomic Rank ◽

Mtdna Sequence ◽

In The Wild

SummaryAn historical study shows that the present day ex situ population of Edwards's Pheasant Lophura edwardsi, now numbering over 1,000 living specimens, originated in the 1920s from at least six different sources and c. 30 potential founders, including more males than females. Partial sequences, 820 nucleotides long, of the mitochondrial DNA (mtDNA) control-region were obtained in representatives of about half of 21 captive-reared bloodlines, identified from data in the revised International Studbook. All captive-reared birds had identical sequences. Sequences of mtDNA obtained from museum skins and samples of birds collected in the wild were slightly different from that representing the captivereared birds. The lack of mtDNA variability in the captive stock is probably due to the small number of founding females and genetic drift during c. 30 generations of captive breeding. Estimation of true extent of mtDNA sequence variability in historical and living wild Edwards's Pheasants awaits the procurement and analysis of more specimens. At least one bloodline of captive Edwards's Pheasant is polluted with exogenous genes resulting from past hybridization with Swinhoe's Pheasant L. sivinhoii. Edwards's Pheasant is more closely related to Vietnamese Pheasant L. hatinhensis and Imperial Pheasant L. imperialis than to several other taxa regarded as full species in the genus Lophura. However it is not yet possible to determine the extent of their evolutionary divergence and of their proper taxonomic rank. The initial results of this genetic research suggest that there should be efforts to (1) expand field sampling and genetic analyses of wild populations of Lophura species, (2) purge the captive stock of Edwards' Pheasant of all hybrids, (3) apply microsatellite analyses to estimate the level of genetic diversity in nuclear DNA.

Download Full-text

Extensive population decline in the Tasmanian devil predates European settlement and devil facial tumour disease

Biology Letters ◽

10.1098/rsbl.2014.0619 ◽

2014 ◽

Vol 10 (11) ◽

pp. 20140619 ◽

Cited By ~ 47

Author(s):

Anna Brüniche-Olsen ◽

Menna E. Jones ◽

Jeremy J. Austin ◽

Christopher P. Burridge ◽

Barbara R. Holland

Keyword(s):

Genetic Diversity ◽

Environmental Changes ◽

Southern Oscillation ◽

Demographic History ◽

Population Decline ◽

Tasmanian Devil ◽

Term Survival ◽

Temporal Sampling ◽

Low Genetic Diversity ◽

Devil Facial Tumour Disease

The Tasmanian devil ( Sarcophilus harrisii ) was widespread in Australia during the Late Pleistocene but is now endemic to the island of Tasmania. Low genetic diversity combined with the spread of devil facial tumour disease have raised concerns for the species’ long-term survival. Here, we investigate the origin of low genetic diversity by inferring the species' demographic history using temporal sampling with summary statistics, full-likelihood and approximate Bayesian computation methods. Our results show extensive population declines across Tasmania correlating with environmental changes around the last glacial maximum and following unstable climate related to increased ‘El Niño–Southern Oscillation’ activity.

Download Full-text