A transmissible cancer shifts from emergence to endemism in Tasmanian devils

Patton, Austin H.; Lawrance, Matthew F.; Margres, Mark J.; Kozakiewicz, Christopher P.; Hamede, Rodrigo; Ruiz‐Aravena, Manuel; Hamilton, David G.; Comte, Sébastien; Ricci, Lauren; Taylor, Rennae S.; Stadler, Tanja; Leaché, Adam D.; McCallum, Hamish; Jones, Menna Lloyd; Hohenlohe, Paul A.; Storfer, Andrew

doi:10.1126/science.abb9772

Cited by 29 publications

(90 citation statements)

References 63 publications

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“…We also found neoplastic mussels without genetic chimerism suggesting the presence of conventional non-transmissible cancers.The analysis of the genotype of 6 tumors from M. edulis hosts confirmed the M. trossulus origin of MtrBTN2 but with an excess of M. edulis-state SNP alleles compared to MtrBTN1 and the M. trossulus population we analysed, or a deficit compared to the highly introgressed M. trossulus population of the Baltic Sea. We surprisingly observed a high amount of nuclear and mitochondrial polymorphism in MtrBTN2 samples which defines two sub-lineages that co-exist and spread in the same populations, as it has been observed in other transmissible cancers(CTVT : Baez-Ortega et al 2019, DFTD: Kwon et al 2020, Patton et al 2020.…”

supporting

confidence: 66%

“…In Tasmanian devils two independent transmissible cancers lineages have emerged in the last 30 years. In bother cases, although at different spatiotemporal scales, genome studies have shown early diversification into sublineages and secondary co-existence of some divergent sublineages (Baez-Ortega et al 2019, Kwon et al 2020Patton et al 2020). Studies in marine bivalves also showed multiple emergences (two in Cerastoderma edule, Metzger et al 2016 and two in Mytilus trossulus, Yonemitsu et al 2019) and for the first time in transmissible cancer research, transmissions crossing the species barrier (BTN lineage in Polititapes aureus has a Venerupis corrugata origin, Metzger et al 2016, and MtrBTN2 in M. edulis and M. chilensis has a M. trossulus origin, Yonemitsu et al 2019).…”

Section: Introductionmentioning

confidence: 99%

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Prevalence and polymorphism of a mussel transmissible cancer in Europe

Hammel

Simon

Arbiol

et al. 2021

Preprint

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Transmissible cancers are parasitic malignant cell lineages that acquired the ability to infect new hosts from the same species, or sometimes related species. First described in dogs and Tasmanian devils, transmissible cancers were later discovered in some marine bivalves affected by a leukemia-like disease. In Mytilus mussels, two lineages of Bivalve Transmissible Neoplasia (BTN), both emerged in a M. trossulus founder individual, have been described to date (MtrBTN1 and MtrBTN2). Here, we performed an extensive screening of genetic chimerism, a hallmark of transmissible cancer, by genotyping hundred SNPs of thousands of European Mytilus mussels. The genetic analysis allowed us to simultaneously obtain the genotype of hosts -M. edulis, M. galloprovincialis or hybrids- and the genotype of tumors of heavily infected individuals. In addition, a subset of individuals were systematically genotyped and analysed by histology in order to screen for possible non-transmissible cancers. We detected MtrBTN2 at low prevalence in M. edulis, and also in M. galloprovincialis and hybrids although at a much lower prevalence. No MtrBTN1 or new BTN were found but a few individuals with non-transmissible neoplasia were observed at a single polluted site on the same sampling date. We observed a diversity of MtrBTN2 genotypes that appeared more introgressed or more ancestral than MtrBTN1 and reference healthy M. trossulus individuals. The observed polymorphism is most likely due to somatic null alleles caused by structural variations or point mutations in primer-binding sites leading to enhanced detection of the host alleles. Despite low prevalence, two divergent sublineages, confirmed by mtCOI sequences, are co-spreading in the same geographic area, suggesting a complex diversification of MtrBTN2 since its emergence and host species shift.

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supporting

confidence: 66%

Section: Introductionmentioning

confidence: 99%

Prevalence and polymorphism of a mussel transmissible cancer in Europe

Hammel

Simon

Arbiol

et al. 2021

Preprint

View full text Add to dashboard Cite

show abstract

“…We surprisingly observed a high amount of nuclear and mitochondrial polymorphism in MtrBTN2 samples. This polymorphism defines two sublineages that co-exist and spread in the same populations, as it has been observed in other transmissible cancers (CTVT: Baez-Ortega et al 2019, DFTD: Kwon et al 2020, Patton et al 2020.…”

Section: Discussionmentioning

confidence: 73%

Prevalence and polymorphism of a mussel transmissible cancer in Europe

et al. 2021

View full text Add to dashboard Cite

Transmissible cancers are parasitic malignant cell lineages that acquired the ability to infect new hosts from the same species, or sometimes related species. First described in dogs and Tasmanian devils, transmissible cancers were later discovered in some marine bivalves affected by a leukemia-like disease. In Mytilus mussels, two lineages of Bivalve Transmissible Neoplasia (BTN) have been described to date (MtrBTN1 and MtrBTN2), both emerged in a M. trossulus founder individual. Here, we performed an extensive screening of genetic chimerism, a hallmark of transmissible cancer, by genotyping 106 SNPs of 5907 European Mytilus mussels. The genetic analysis allowed us to simultaneously obtain the genotype of hosts -M. edulis, M. galloprovincialis or hybrids -and the genotype of tumors of heavily infected individuals. In addition, a subset of 222 individuals were systematically genotyped and analysed by histology in order to screen for possible non-transmissible cancers. We detected MtrBTN2 at low prevalence in M.edulis, and also in M. galloprovincialis and hybrids although at a much lower prevalence. No MtrBTN1 or new BTN were found, but 8 individuals with non-transmissible neoplasia were observed at a single polluted site on the same sampling date. We observed a diversity of MtrBTN2 genotypes that appeared more introgressed or more ancestral than MtrBTN1 and reference healthy M. trossulus individuals. The observed polymorphism is most likely due to somatic null alleles caused by structural variations or point mutations in primer-binding sites leading to enhanced detection of the host alleles. Despite low prevalence, two sublineages divergent by 10% fixed somatic null alleles and one non-synonymous mtCOI substitution, are co-spreading in the same geographic area, suggesting a complex diversification of MtrBTN2 since its emergence and host species shift.

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“…If DFTD persists long-term in the devil population with ongoing coevolution, it may lead to diversifying selection for specific, qualitative host resistance mechanisms [83]. Indeed, phylodynamic analysis of DFTD as it spread across Tasmania supports the hypothesis that devils may be mounting a response; transmission rates have decayed such that DFTD appears to be shifting from emergence to endemism [85]. Although host-genomic variation was not jointly considered in that study, the combined evidence of multiple studies demonstrating rapid evolutionary response of devils to DFTD, including this one, support these interpretations.…”

Section: (C) Comparing Contemporary and Historical Time Scalesmentioning

confidence: 94%

“…The widespread contemporary evolution we found in devils reflects the recent prediction [83] that response to an emergent disease is most likely to be controlled by many genes conferring quantitative resistance [84], for example, by reducing the within-host growth rate of tumours. DFTD is predicted to become less virulent in the short-term [31,85]. If DFTD persists long-term in the devil population with ongoing coevolution, it may lead to diversifying selection for specific, qualitative host resistance mechanisms [83].…”

Section: (C) Comparing Contemporary and Historical Time Scalesmentioning

confidence: 99%

Contemporary and historical selection in Tasmanian devils ( Sarcophilus harrisii ) support novel, polygenic response to transmissible cancer

et al. 2021

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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.

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A transmissible cancer shifts from emergence to endemism in Tasmanian devils

Cited by 29 publications

References 63 publications

Prevalence and polymorphism of a mussel transmissible cancer in Europe

Prevalence and polymorphism of a mussel transmissible cancer in Europe

Prevalence and polymorphism of a mussel transmissible cancer in Europe

Contemporary and historical selection in Tasmanian devils ( Sarcophilus harrisii ) support novel, polygenic response to transmissible cancer

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