Pearl farmers routinely graft tissue from one oyster into another, and more than 90% of the time the recipient does not reject it—a sign that bivalve molluscs may lack a basic immune ability that most other animals possess. This matters because the same poor self/non-self recognition may explain why bivalves have spawned at least eight distinct lineages of transmissible cancer—cancers that spread between individuals like an infection. In vertebrates, such cancers are vanishingly rare (only three lineages known, in Tasmanian devils and dogs), and each has been linked to a weakened allorecognition system. If the team’s hypothesis holds, bivalves could become a natural model for understanding how cancers evolve to evade immune detection. The project is fundamental science: it probes the rules of life by testing when and why bivalve tissues reject each other, both in the lab and in living animals, and by sequencing the genomes of transmissible cancer cells. There is no immediate practical application, but a deeper grasp of allorecognition could eventually inform bivalve aquaculture—helping breeders select for disease-resistant stocks—and reshape how biologists think about the evolution of immunity and contagious cancers across the animal kingdom.
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The advent of multicellularity was a critical evolutionary step that occurred several times independently, leading to the evolution of animals, plants, fungi, and some algae. The ability of cells to discriminate ‘self’ from ‘non-self’ (and, particularly, the ability to detect ‘self’ from conspecific ‘non-self’ - allorecognition) is thought to have been fundamental for this evolution, ensuring genetic stability by preventing the formation of chimeras. Self/non-self recognition is also important for embryonic development, wound-healing, and immune responses, and is therefore thought to be an essential property of multicellular organisms. Our proposed project stems from observations by our team and others that, surprisingly, capacity for allorecognition may be limited in bivalve molluscs. For example, cultured pearl formation involves tissue grafts between two individuals of the same species, and we regularly observe graft success rates that exceed 90%. Another line of evidence for poor allorecognition in bivalves is the recent discovery of eight distinct transmissible neoplasia (cancer) lineages in a range of bivalve species. Transmissible cancers are incredibly rare; besides bivalves, detection has been limited to two cancer lineages within Tasmanian devils, and one in canines. In both these vertebrate systems the cancers have been linked to a dampened allorecognition system, suggesting a link between suppression of allorecognition and evolution of transmissible cancer. We hypothesise that allorecognition is impaired in bivalve molluscs, and that this impairment may explain the repeated evolution of transmissible neoplasia in this group of animals. We aim to test this hypothesis by conducting nested experiments using tissues from the same individual, different individuals from the same species, and individuals of different species (using combinations of both closely and distantly-related species) to determine when tissue rejection occurs. These experiments will be conducted both in-vitro and in-vivo, and will be coupled with analysis of gene expression to identify the molecular components involved in self/non-self recognition. Finally, we will analyse the genomes of bivalve transmissible neoplasia cells to explore whether a lack of allorecognition may explain their repeated independent evolution. This study directly aligns with the BBSRC’s research priority ‘advancing the frontiers of bioscience: understanding the rules of life’. It aims to reveal the fundamental nature of the mechanisms for recognition of non-self in a major group of marine animals, providing a better understanding of bivalve immunity and potentially initiating a major re-evaluation of our understanding of the ubiquity of allorecognition in animals. Knowledge gained in this project will benefit bivalve aquaculture and restoration programmes, facilitating further research on the role of genetic diversity of populations in resilience to transmissible cancer outbreaks. The project will also reveal fundamental principles governing the evolution of transmissible cancers.
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