Multiple lineages of transmissible neoplasia in the basket cockle (Clinocardium nuttallii) with repeated horizontal transfer of mitochondrial DNA

Transmissible cancers are clonal lineages of neoplastic cells able to infect multiple hosts, spreading through the environment as an infectious disease. Transmissible cancers have been identified in Tasmanian devils, dogs, and bivalves. Several lineages of bivalve transmissible neoplasias (BTN) have been identified in multiple bivalve species. In 2019 in Puget Sound, disseminated neoplasia was observed in basket cockles (Clinocardium nuttallii), a species that is important to the culture and diet of the Suquamish Tribe as well as other tribes with traditional access to the species. To investigate disseminated neoplasia in cockles, a nuclear locus was amplified from a collection of cockles from Agate Pass, and DNA sequences showed evidence of a single cancer lineage, termed CnuBTN1, in three cockles. We used cytology and a qPCR assay targeting sequences found in BTNs to analyze collections of cockles from eleven locations from Puget Sound and the Washington coastline to screen for BTN and identify the extent of cancer spread. Three lineages of BTN in cockles were identified, with CnuBTN1 being the most prevalent and geographically widespread and the others only found in one location each. While multiple nuclear loci show all samples of CnuBTN1 come from a single lineage, the mitochondrial alleles in each cockle with CnuBTN1 are different from each other, suggesting mitochondrial genomes of this cancer have been replaced multiple times during its evolution through horizontal transmission. The identification and analysis of these BTNs are critical for broodstock selection, management practices, and repopulation of declining cockle populations, which will enable the continued cultural connection and dietary use of the cockles by the local Tribes.