Widespread transmission of independent cancer lineages within multiple bivalve species

Abstract

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 distinctive cases in mammals (Tasmanian devils1 and dogs2,3), but these are generally considered to be rare exceptions in nature. The discovery of transmissible cancer in soft-shell clams (Mya arenaria)4 suggested that this phenomenon might be more widespread. Here we analyzed disseminated neoplasia in mussels (Mytilus trossulus), cockles (Cerastoderma edule), and golden carpet shell clams (Polititapes aureus) and found 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, but unexpectedly, cancer cells in P. aureus are all derived from Venerupis corrugata, a different species living in the same geographic 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 were found spreading within the species of origin, cross-species transmission of cancer cells can occur.

Weird genotypes? Don't discard them, transmissible cancer could be an explanation

“…As these two conditions seem more likely to be reached in the marine environment, could transmissible cancer be more frequent in marine invertebrates? The answer has just arrived last June, with transmissible cancers identified in multiple marine bivalve species (Metzger et al., 2016). In addition to the previously reported case in M. arenaria , hallmarks of transmissible cancers have been found in Mytilus trossulus mussels, in Cerastoderma edule cockles, and in the golden carpet‐shell clam Polititapes aureus (Metzger et al., 2016).…”

“…The answer has just arrived last June, with transmissible cancers identified in multiple marine bivalve species (Metzger et al., 2016). In addition to the previously reported case in M. arenaria , hallmarks of transmissible cancers have been found in Mytilus trossulus mussels, in Cerastoderma edule cockles, and in the golden carpet‐shell clam Polititapes aureus (Metzger et al., 2016). These marine bivalves are far from genetically depleted as Tasmanian devil and dog breeds were suspected to be.…”

“…1 in Metzger et al., 2016). In addition, genetic similarities between cancer cell DNA of different individuals attests infection by the same clone and genetic differences allow identifying cancer lineages that must have emerged independently, as found in Tasmanian devil (Pye et al., 2016) and cockles (Metzger et al., 2016). …”

“…Prior to Metzger et al. (2016) publication, infectious cancer would unlikely be considered. Two mitochondrial sequences would most likely be interpreted as contamination or heteroplasmy possibly due to paternal leaking.…”

“…(2016)'s publication appeared while we were having difficulties to interpret weird genotypes in our Mytilus mussel dataset. Among 938 mussels sampled along the European Atlantic coasts (from the Netherlands to France), we found what we thought to be five hybrid genotypes between M. edulis and M. trossulus , one in the Wadden Sea, one in Barfleur, one in Pornichet, and the other two in Arcachon (see samples 1, 13, 27 and 31 in the map, Figure 1).…”