scholarly journals Historical and contemporary signatures of selection in response to transmissible cancer in the Tasmanian Devil (Sarcophilus harrisii)

Author(s):  
Amanda R. Stahlke ◽  
Brendan Epstein ◽  
Soraia Barbosa ◽  
Austin Patton ◽  
Sarah A. Hendricks ◽  
...  

AbstractTasmanian devils (Sarcophilus harrisii) are evolving in response to a unique transmissible cancer, devil facial tumour disease (DFTD), first described in 1996. Persistence of wild populations and the recent emergence of a second independently evolved transmissible cancer suggest that transmissible cancers may be a recurrent feature in devils. We used a targeted sequencing approach, RAD-capture, to identify genomic regions subject to rapid evolution in approximately 2,500 devils as DFTD spread across the species range. We found evidence for genome-wide contemporary evolution, including 186 candidate genes related to cell cycling and immune response. We then searched for signatures of recurrent selection with a molecular evolution approach and found widespread evidence of historical positive selection in devils relative to other marsupials. We identified both contemporary and historical selection in 19 genes and enrichment for contemporary and historical selection independently in 22 gene sets. Nonetheless, the overlap between candidates for historical selection and for contemporary response to DFTD was lower than expected, supporting novelty in the evolutionary response of devils to DFTD. Our results can inform management actions to conserve adaptive capacity of devils by identifying high priority targets for genetic monitoring and maintenance of functional diversity in managed populations.

2021 ◽  
Vol 288 (1951) ◽  
pp. 20210577
Author(s):  
Amanda R. Stahlke ◽  
Brendan Epstein ◽  
Soraia Barbosa ◽  
Mark J. Margres ◽  
Austin H. Patton ◽  
...  

Tasmanian devils ( Sarcophilus harrisii ) are evolving in response to a unique transmissible cancer, devil facial tumour disease (DFTD), first described in 1996. Persistence of wild populations and the recent emergence of a second independently evolved transmissible cancer suggest that transmissible cancers may be a recurrent feature in devils. Here, we compared signatures of selection across temporal scales to determine whether genes or gene pathways under contemporary selection (six to eight generations) have also been subject to historical selection (65–85 Myr). First, we used targeted sequencing, RAD-capture, in approximately 2500 devils in six populations to identify genomic regions subject to rapid evolution. We documented genome-wide contemporary evolution, including 186 candidate genes related to cell cycling and immune response. Then we used a molecular evolution approach to identify historical positive selection in devils compared to other marsupials and found evidence of selection in 1773 genes. However, we found limited overlap across time scales, with only 16 shared candidate genes, and no overlap in enriched functional gene sets. Our results are consistent with a novel, multi-locus evolutionary response of devils to DFTD. Our results can inform conservation by identifying high priority targets for genetic monitoring and guiding maintenance of adaptive potential in managed populations.


2017 ◽  
Vol 4 (4) ◽  
pp. 170053 ◽  
Author(s):  
Lauren C. White ◽  
Jeremy J. Austin

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.


2021 ◽  
Author(s):  
Camila Espejo ◽  
Richard Wilson ◽  
Ruth J. Pye ◽  
Julian C. Ratcliffe ◽  
Manuel Ruiz-Aravena ◽  
...  

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.


2018 ◽  
Vol 58 (6) ◽  
pp. 1043-1054 ◽  
Author(s):  
Gregory M Woods ◽  
Samantha Fox ◽  
Andrew S Flies ◽  
Cesar D Tovar ◽  
Menna Jones ◽  
...  

AbstractThe Tasmanian devil, a marsupial carnivore, has been restricted to the island state of Tasmania since its extinction on the Australian mainland about 3000 years ago. In the past two decades, this species has experienced severe population decline due to the emergence of devil facial tumor disease (DFTD), a transmissible cancer. During these 20 years, scientists have puzzled over the immunological and evolutionary responses by the Tasmanian devil to this transmissible cancer. Targeted strategies in population management and disease control have been developed as well as comparative processes to identify variation in tumor and host genetics. A multi-disciplinary approach with multi-institutional teams has produced considerable advances over the last decade. This has led to a greater understanding of the molecular pathogenesis and genomic classification of this cancer. New and promising developments in the Tasmanian devil’s story include evidence that most immunized, and some wild devils, can produce an immune response to DFTD. Furthermore, epidemiology combined with genomic studies suggest a rapid evolution to the disease and that DFTD will become an endemic disease. Since 1998 there have been more than 350 publications, distributed over 37 Web of Science categories. A unique endemic island species has become an international curiosity that is in the spotlight of integrative and comparative biology research.


EcoHealth ◽  
2007 ◽  
Vol 4 (3) ◽  
pp. 338-345 ◽  
Author(s):  
Gregory M. Woods ◽  
Alexandre Kreiss ◽  
Katherine Belov ◽  
Hannah V. Siddle ◽  
David L. Obendorf ◽  
...  

Pathogens ◽  
2020 ◽  
Vol 9 (11) ◽  
pp. 873
Author(s):  
Siobhon L. Egan ◽  
Manuel Ruiz-Aravena ◽  
Jill M. Austen ◽  
Xavier Barton ◽  
Sebastien Comte ◽  
...  

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.


2018 ◽  
Vol 285 (1891) ◽  
pp. 20182239 ◽  
Author(s):  
Manuel Ruiz-Aravena ◽  
Menna E. Jones ◽  
Scott Carver ◽  
Sergio Estay ◽  
Camila Espejo ◽  
...  

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.


2019 ◽  
Vol 31 (7) ◽  
pp. 1296 ◽  
Author(s):  
C. E. Grueber ◽  
E. Peel ◽  
B. Wright ◽  
C. J. Hogg ◽  
K. Belov

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.


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