Widespread transmission of independent cancer lineages within multiple bivalve species

Most cancers arise from oncogenic changes in the genomes of somatic cells, and while the cells may migrate by metastasis, they remain within that single individual. Natural transmission of cancer cells from one individual to another has been observed in two distinct cases in mammals (Tasmanian devils and dogs), but these are generally considered to be rare exceptions in nature. The discovery of transmissible cancer in soft-shell clams (Mya arenaria) suggested that this phenomenon might be more widespread. Here we analyse disseminated neoplasia in mussels (Mytilus trossulus), cockles (Cerastoderma edule), and golden carpet shell clams (Polititapes aureus) and find that neoplasias in all three species are attributable to independent transmissible cancer lineages. In mussels and cockles, the cancer lineages are derived from their respective host species; however, unexpectedly, cancer cells in P. aureus are all derived from Venerupis corrugata, a different species living in the same geographical area. No cases of disseminated neoplasia have thus far been found in V. corrugata from the same region. These findings show that transmission of cancer cells in the marine environment is common in multiple species, that it has originated many times, and that while most transmissible cancers are found spreading within the species of origin, cross-species transmission of cancer cells can occur.

• Publication year

  2016

• Venue

  Nature

• Publication date

  2016-06-05

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1038/nature18599PMID 27338791PMCID 4939143
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• Cancer cells in Polititapes aureus are derived from Venerupis corrugata, showing that cross-species transmission can occur in bivalve cancers.

  Confidence 0.97

  박진우 (dztg5apj7m) extractionB (s683577b42) reviewjihoonc (k5vuy3tzcm) reviewAK (4715169a40) review
• The cancer lineages in mussels and cockles are derived from their respective host species.

  Confidence 0.95

  박진우 (dztg5apj7m) extractionB (s683577b42) reviewjihoonc (k5vuy3tzcm) reviewAK (4715169a40) review
• Disseminated neoplasias in mussels, cockles, and golden carpet shell clams are attributable to independent transmissible cancer lineages.

  Confidence 0.98

  박진우 (dztg5apj7m) extractionB (s683577b42) reviewjihoonc (k5vuy3tzcm) reviewAK (4715169a40) review

• cerastoderma edule

  species

  A cockle species analyzed for disseminated neoplasia in the study.

  Aliases: cockles

  박진우 (dztg5apj7m) extractionB (s683577b42) reviewjihoonc (k5vuy3tzcm) reviewAK (4715169a40) review
• cross-species transmission

  process, phenomenon

  Transfer of cancer cells from one species to another.

  박진우 (dztg5apj7m) extractionB (s683577b42) reviewjihoonc (k5vuy3tzcm) reviewAK (4715169a40) review
• disseminated neoplasia

  condition

  A systemic bivalve disease characterized by widespread proliferation of abnormal cells through the body.

  박진우 (dztg5apj7m) extractionB (s683577b42) reviewjihoonc (k5vuy3tzcm) reviewAK (4715169a40) review
• mytilus trossulus

  species

  A mussel species analyzed for disseminated neoplasia in the study.

  Aliases: mussels

  박진우 (dztg5apj7m) extractionB (s683577b42) reviewjihoonc (k5vuy3tzcm) reviewAK (4715169a40) review
• polititapes aureus

  species

  A golden carpet shell clam species analyzed for disseminated neoplasia in the study.

  Aliases: golden carpet shell clam

  박진우 (dztg5apj7m) extractionB (s683577b42) reviewjihoonc (k5vuy3tzcm) reviewAK (4715169a40) review
• transmissible cancer lineage

  lineage

  A clonal population of cancer cells capable of spreading between individual hosts.

  Aliases: transmissible cancer

  박진우 (dztg5apj7m) extractionB (s683577b42) reviewjihoonc (k5vuy3tzcm) reviewAK (4715169a40) review
• venerupis corrugata

  species

  A bivalve species living in the same region and identified as the source species for cancer cells found in Polititapes aureus.

  박진우 (dztg5apj7m) extractionB (s683577b42) reviewjihoonc (k5vuy3tzcm) reviewAK (4715169a40) review

• Long-term epidemiological study of disseminated neoplasia of cockles in Galicia (NW Spain): temporal patterns at individual and population levels, influence of environmental and cockle-based factors and lethality.

  2016cited by this paper
• Field and laboratory transmission studies of haemic neoplasia in the soft-shell clam, Mya arenaria, from Atlantic Canada.

  2016cited by this paper
• NOAA National Centers for Coastal Ocean Science Center for Coastal Monitoring and Assessment

  2015cited by this paper
• Neoplastic diseases of marine bivalves.

  2015cited by this paper
• Malignant Transformation of Hymenolepis nana in a Human Host.

  2015cited by this paper
• Estudio patológico de las poblaciones de berberecho Cerastoderma edule (L.) de Galicia

  2015cited by this paper
• A second transmissible cancer in Tasmanian devils

  2015cited by this paper
• Horizontal transmission of clonal cancer cells causes leukemia in soft-shell clams.

  2015cited by this paper
• The changing global distribution and prevalence of canine transmissible venereal tumour

  2014cited by this paper
• Using flow cytometry to detect haemic neoplasia in mussels (Mytilus trossulus) from the Pacific Coast of Southern British Columbia, Canada.

  2014cited by this paper
• Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction

  2014cited by this paper
• Activation of transcription and retrotransposition of a novel retroelement, Steamer, in neoplastic hemocytes of the mollusk Mya arenaria

  2014cited by this paper
• Disseminated neoplasia in clams Venerupis aurea from Galicia (NW Spain): histopathology, ultrastructure and ploidy of the neoplastic cells, and comparison of diagnostic procedures.

  2013cited by this paper
• Molecular phylogenetics in 2D: ITS2 rRNA evolution and sequence-structure barcode from Veneridae to Bivalvia.

  2012cited by this paper
• New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.

  2010cited by this paper
• Expression of mutant protein p53 and Hsp70 and Hsp90 chaperones in cockles Cerastoderma edule affected by neoplasia.

  2010cited by this paper
• Variations in p53-like cDNA sequence are correlated with mussel haemic neoplasia: A potential molecular-level tool for biomonitoring.

  2010cited by this paper
• Origins and Evolution of a Transmissible Cancer

  2009cited by this paper
• Development of twelve polymorphic microsatellite markers in the edible cockle Cerastoderma edule (Bivalvia: Cardiidae)

  2009cited by this paper
• Cardiidae

  2008cited by this paper
• Invertebrate p53-like mRNA isoforms are differentially expressed in mussel haemic neoplasia.

  2008cited by this paper
• Clonal origin and evolution of a transmissible cancer.

  2006cited by this paper
• Allograft theory: Transmission of devil facial-tumour disease

  2006cited by this paper
• Neoplastic diseases of commercially important marine bivalves

  2004cited by this paper
• Molecular data from the 16S rRNA gene for the phylogeny of Veneridae (Mollusca: Bivalvia)

  2003cited by this paper
• Inheritance of microsatellite loci in the white sturgeon (Acipenser transmontanus).

  2002cited by this paper
• Contrasting morphological and molecular variation in Coralliophila meyendorffii (Muricidae, Coralliophilinae)

  2001cited by this paper
• Parasites and pathologic conditions of the cockle Cerastoderma edule populations of the coast of Galicia (NW Spain).

  2001cited by this paper
• Disseminated neoplasia and large foci indicating heavy haemocytic infiltration in cockles Cerastoderma edule from Galicia (NW Spain).

  2001cited by this paper
• DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates.

  1994cited by this paper
• Alternate pathogenesis of systemic neoplasia in the bivalve mollusc Mytilus.

  1991cited by this paper
• Failure of transmission of hemic neoplasia of bay mussels, Mytilus trossulus, to other bivalve species.

  1991cited by this paper
• Transmission of transmissible venereal tumor of the dog to the coyote.

  1979cited by this paper
• Transplantables Rundzellensarkom des Hundes

  1906cited by this paper
• An experimental investigation of infective sarcoma of the dog, with a consideration of its relationship to cancer

  year unknowncited by this paper

• Metabolic pathways fuelling Devil Facial Tumour Disease

  2026cites this paper
• Harmonized nonhuman cancer database

  2025cites this paper
• Epidemiological insight into disseminated neoplasia in Mytilus chilensis from southern Chile.

  2025cites this paper
• Prevalence of hemic neoplasia in cockles and co-habiting bivalve species in the western coast of France and the southern coast of Portugal

  2025cites this paper
• Scanning the horizon: anticipating future changes in Portuguese aquatic ecosystems

  2025cites this paper
• External immune sentinels in the seawater ecosystem: the specialization of bivalve hemocytes.

  2025cites this paper
• Gene expression in soft-shell clam (Mya arenaria) transmissible cancer reveals survival mechanisms during host infection and seawater transfer

  2025cites this paper
• Variation in natural infection outcomes and cancer cell release from soft-shell clams (Mya arenaria) with bivalve transmissible neoplasia

  2025cites this paper
• Micro-to multi-chimerism: the multiple facets of a singular phenomenon

  2025cites this paper
• Ecology of vertical tumor transmission in the freshwater cnidarian Hydra oligactis

  2025cites this paper
• Marteilia cocosarum in the Wash Estuary, UK: links to mass mortalities of cockles Cerastoderma edule and relationship to closely related species.

  2025cites this paper
• Characterisation of Marteilia cocosarum in the Wash Estuary, UK, linked to mass mortalities of cockles (Cerastoderma edule), and its relationship to closely related species

  2025cites this paper
• No Evidence for Distinct Transcriptomic Subgroups of Devil Facial Tumor Disease (DFTD)

  2025cites this paper
• Applying multilevel selection to understand cancer evolution and progression

  2025cites this paper
• Widespread HCD-tRNA derived SINEs in bivalves rely on multiple LINE partners and accumulate in genic regions

  2024cites this paper
• Marine transmissible cancer navigates urbanized waters, threatening spillover

  2024cites this paper
• A brief global agenda for advancing the study of molluscs

  2024cites this paper
• Oncogenic processes: a neglected parameter in the evolutionary ecology of animals.

  2024cites this paper
• Engineering an energy-dissipating hybrid tissue in vivo for obesity treatment.

  2024cites this paper
• Application of Hemolymph Smear Histology Diagnosis to Detect Disseminated Neoplasia in Basket Cockles (Clinocardium nuttallii)

  2024cites this paper
• Gene expression in soft-shell clam (Mya arenaria) transmissible cancer reveals survival mechanisms during host infection and seawater transfer

  2024cites this paper
• The chromosome level genome assembly of the Asian green mussel, Perna viridis

  2024cites this paper
• Unravelling epigenetic mechanisms in Cerastoderma edule genome: a comparison of healthy and neoplastic cockles

  2024cites this paper
• Transmissible cancers, the genomes that don't melt down.

  2024cites this paper
• De novo evolution of transmissible tumours in hydra

  2024cites this paper
• Identification of an Outbreak of Bivalve Transmissible Neoplasia in Soft-Shell Clams (Mya arenaria) in the Puget Sound Using Hemolymph and eDNA Surveys

  2024cites this paper
• Multiple lineages of transmissible neoplasia in the basket cockle (C. nuttallii) with repeated horizontal transfer of mitochondrial DNA

  2024influential citation
• Novel PCR assay for the identification of two transmissible cancers in Cerastoderma edule.

  2024cites this paper
• From shells to sequences: A proof-of-concept study for on-site analysis of hemolymphatic circulating cell-free DNA from sentinel mussels using Nanopore technology.

  2024cites this paper
• Plethora of New Marsupial Genomes Informs Our Knowledge of Marsupial MHC Class II

  2024cites this paper
• De novo evolution of transmissible tumors in Hydra

  2024cites this paper
• In vitro competition between two transmissible cancers and potential implications for their host, the Tasmanian devil

  2024cites this paper
• Age-Related and Seasonal Dynamics of the Hemocyte Population in the Mussel Crenomytilus grayanus (Dunker, 1853)

  2023cites this paper
• A rapid, inexpensive, non-lethal method for detecting disseminated neoplasia in a bivalve

  2023cites this paper
• Chromosome-Level Genome Assembly of the Blue Mussel Mytilus chilensis Reveals Molecular Signatures Facing the Marine Environment

  2023cites this paper
• Disseminated neoplasia in cultured hard clams (Mercenaria mercenaria)

  2023cites this paper
• The Mystery of Cancer Resistance: A Revelation Within Nature

  2023cites this paper
• Transcriptomics of mussel transmissible cancer MtrBTN2 suggests accumulation of multiple cancer traits and oncogenic pathways shared among bilaterians

  2023cites this paper
• A chromosome-level genome for the nudibranch gastropod Berghia stephanieae helps parse clade-specific gene expression in novel and conserved phenotypes

  2023cites this paper
• SNP discovery and genetic structure in blue mussel species using low coverage sequencing and a medium density 60 K SNP‐array

  2023cites this paper
• Molecular diversity of bivalve transmissible neoplasia of blue mussels in the Kola Bay (Barents Sea) indicates a recent migration of the cancer lineages between the North Pacific and Northern Europe

  2023cites this paper
• Marine transmissible cancer navigates urbanised waters, threatening to spillover

  2023cites this paper
• Contagious Cancers That Can Spread Between Ocean Organisms

  2023cites this paper
• Age-Related and Seasonal Dynamics of Hemocyte Population in the Mussel Crenomytilus grayanus (Dunker, 1853)

  2023cites this paper
• The effect of mitochondrial recombination on fertilization success in blue mussels.

  2023cites this paper
• Genetic features of bivalve transmissible neoplasia in blue mussels from the Kola Bay (Barents Sea) suggest a recent trans‐Arctic migration of the cancer lineages

  2023influential citation
• Multiple lineages of transmissible neoplasia in the basket cockle ( Clinocardium nuttallii ) with 1 repeated horizontal transfer of mitochondrial DNA 2

  2023influential citation
• Somatic evolution of marine transmissible leukemias in the common cockle, Cerastoderma edule

  2023cites this paper
• Title: A rapid, inexpensive, non-lethal method for detecting 1 disseminated neoplasia in a bivalve. 2

  2023cites this paper
• Centuries of genome instability and evolution in soft-shell clam, Mya arenaria, bivalve transmissible neoplasia

  2023cites this paper
• Genetic divergence of farmed blue mussels (Mytilus sp.) in Australian waters

  2023cites this paper
• Is chimerism associated with cancer across the tree of life?

  2023cites this paper
• Mitochondrial genome sequencing of marine leukaemias reveals cancer contagion between clam species in the Seas of Southern Europe

  2022cites this paper
• Transmissible Cancer Evolution: The Under-Estimated Role of Environmental Factors in the “Perfect Storm” Theory

  2022influential citation
• Two lineages of bivalve transmissible neoplasia affect the blue mussel Mytilus trossulus Gould in the subarctic Sea of Okhotsk

  2022cites this paper
• Two branchial pathological conditions, nuclear hypertrophy and abnormal epithelial proliferation, in Mya arenaria from northwest Russian coasts.

  2022cites this paper
• Comparative analysis of the Mercenaria mercenaria genome provides insights into the diversity of transposable elements and immune molecules in bivalve mollusks

  2022cites this paper
• Синдром Карпентера: бессмертные линии трансмиссивного рака меняют своих смертных хозяев, "Природа"

  2022cites this paper
• Applying the concept of liquid biopsy to monitor the microbial biodiversity of marine coastal ecosystems

  2022cites this paper
• The evolution of two transmissible leukaemias colonizing the coasts of Europe

  2022cites this paper
• Centuries of genome instability and evolution in soft-shell clam transmissible cancer

  2022cites this paper
• A review of the methods used to induce cancer in invertebrates to study its effects on the evolution of species and ecosystem functioning

  2022cites this paper
• Development of a semi-quantitative scoring protocol for gill lesion assessment in greenlip abalone Haliotis laevigata held at elevated water temperature.

  2022cites this paper
• Population genetics of clonally transmissible cancers

  2022cites this paper
• Horizontal transmission of disseminated neoplasia in the widespread clam Macoma balthica from the Southern Baltic Sea

  2022cites this paper
• Etiologías asociadas con neoplasias diseminadas en moluscos bivalvos

  2022cites this paper
• The native mussel Mytilus chilensis genome reveals adaptative molecular signatures facing the marine environment

  2022cites this paper
• Two fingerprinting sets for Humulus lupulus based on KASP and microsatellite markers

  2022cites this paper
• Survival and Detection of Bivalve Transmissible Neoplasia from the Soft-Shell Clam Mya arenaria (MarBTN) in Seawater

  2021cites this paper
• Searching for transmissible cancers among the mussels of Europe

  2021cites this paper
• Traits of a mussel transmissible cancer are reminiscent of a parasitic life style

  2021cites this paper
• The genome of the zebra mussel, Dreissena polymorpha: a resource for comparative genomics, invasion genetics, and biocontrol

  2021cites this paper
• Group phenotypic composition in cancer

  2021cites this paper
• NEOPLASIA

  2021cites this paper
• Evolutionary Transformations of the Metazoan Body Plan: Genomic-Morphogenetic Correlations

  2021cites this paper
• Linking pollution and cancer in aquatic environments: A review.

  2021cites this paper
• Between the Devil and the Deep Blue Sea: Non-Coding RNAs Associated with Transmissible Cancers in Tasmanian Devil, Domestic Dog and Bivalves

  2021cites this paper
• Machine learning is a powerful tool to study the effect of cancer on species and ecosystems

  2021cites this paper
• The differentiation state of the Schwann cell progenitor drives phenotypic variation between two contagious cancers

  2021cites this paper
• AQUACULTURE

  2021cites this paper
• Diseases, Parasites and the Immune Response

  2021cites this paper
• Reverting to single-cell biology: The predictions of the atavism theory of cancer.

  2021cites this paper
• First description of a widespread Mytilus trossulus-derived bivalve transmissible cancer lineage in M. trossulus itself

  2021cites this paper
• Genotype data not consistent with clonal transmission of sea turtle fibropapillomatosis or goldfish schwannoma

  2021cites this paper
• Long-Term Trends in the Occurrence of Disseminated Neoplasia in a Population of Mya arenaria (Softshell Clam) from a New Hampshire Estuary

  2021cites this paper
• Oncofly: A CURE for Cancer

  2021cites this paper
• A review of the potential effects of climate change on disseminated neoplasia with an emphasis on efficient detection in marine bivalve populations

  2021cites this paper
• What Animal Cancers teach us about Human Biology

  2021cites this paper
• The immunopeptidomes of two transmissible cancers and their host have a common, dominant peptide motif

  2021cites this paper
• High genetic diversity of bivalve transmissible neoplasia in the blue mussel Mytilus trossulus Gould from the subarctic Sea of Okhotsk

  2021influential citation
• Mitochondrial genome sequencing of marine leukemias reveals cancer contagion between clam species in the Seas of Southern Europe

  2021influential citation
• Mobilizing molluscan models and genomes in biology

  2021cites this paper
• Prevalence and polymorphism of a mussel transmissible cancer in Europe

  2021cites this paper
• Biochemical characterisation of potentially contagious haemic neoplasia occurring in the Baltic clam Limecola balthica

  2021cites this paper
• Vibrio aestuarianus subsp. cardii subsp. nov., pathogenic to the edible cockles Cerastoderma edule in France, and establishment of Vibrio aestuarianus subsp. aestuarianus subsp. nov. and Vibrio aestuarianus subsp. francensis subsp. nov.

  2021cites this paper
• Hemocytes released in seawater act as Trojan horses for spreading of bacterial infections in mussels

  2020cites this paper
• Population Genomics of Wildlife Cancer

  2020cites this paper
• Cancer risk landscapes: A framework to study cancer in ecosystems.

  2020cites this paper
• Transmissible cancers and the evolution of sex under the Red Queen hypothesis

  2020cites this paper
• Semimytilus algosus: first known hermaphroditic mussel with doubly uniparental inheritance of mitochondrial DNA

  2020cites this paper