Evolution and lineage dynamics of a transmissible cancer in Tasmanian devils

• DOI: 10.1371/journal.pbio.3000926
• Publication Date: 2020-11-24T23:37:24Z
• Authors: Young Mi Kwon; Kevin Gori; Naomi Park; Nicole Potts; Kate Swift; Jinhong Wang; Maximilian R. Sta...; Naomi Cannell; Adrian Baez-Ortega; Sebastien Comte; Samantha Fox; Colette Harmsen; Stewart Huxtable; Menna Jones; Alexandre Kreiss; Clare Lawrence; Billie Lazenby; Sarah Peck; Ruth Pye; Gregory Woods; Mona Zimmermann; David C. Wedge; David Pemberton; Michael R. Stratton; Rodrigo Hamede; Elizabeth P. Murc...
• Keywords: Male; Medicine and health sciences; FOS: Computer and information sciences; 0301 basic medicine; Computer and information sciences; DNA Copy Number Variations; Biology and life sciences; QH301-705.5; ResearchInstitutes_Networks_Beacons/mcrc; name=Manchester Cancer Research Centre; Genomic Instability; Tasmania; Animal Diseases; 3. Good health; Evolution, Molecular; 03 medical and health sciences; Marsupialia; Tumor Cells, Cultured; Animals; Female; Biology (General); Facial Neoplasms; Phylogeny; Telomere Shortening; Research Article

Devil facial tumour 1 (DFT1) is a transmissible cancer clone endangering the Tasmanian devil. The expansion of DFT1 across Tasmania has been documented, but little is known of its evolutionary history. We analysed genomes of 648 DFT1 tumours collected throughout the disease range between 2003 and 2018. DFT1 diverged early into five clades, three spreading widely and two failing to persist. One clade has replaced others at several sites, and rates of DFT1 coinfection are high. DFT1 gradually accumulates copy number variants (CNVs), and its telomere lengths are short but constant. Recurrent CNVs reveal genes under positive selection, sites of genome instability, and repeated loss of a small derived chromosome. Cultured DFT1 cell lines have increased CNV frequency and undergo highly reproducible convergent evolution. Overall, DFT1 is a remarkably stable lineage whose genome illustrates how cancer cells adapt to diverse environments and persist in a parasitic niche.