Comparison of Reptilian Genomes Reveals Deletions Associated with the Natural Loss of gamma delta T Cells in Squamates

T lymphocytes or T cells are key components of the vertebrate response to pathogens and cancer. There are two T cell classes based on their TCRs, alpha beta T cells and gamma delta T cells, and each plays a critical role in immune responses. The squamate reptiles may be unique among the vertebrate lineages by lacking an entire class of T cells, the gamma delta T cells. In this study, we investigated the basis of the loss of the gamma delta T cells in squamates. The genome and transcriptome of a sleepy lizard, the skink Tiliqua rugosa, were compared with those of tuatara, Sphenodon punctatus, the last living member of the Rhynchocephalian reptiles. We demonstrate that the lack of TCR gamma and TCR delta transcripts in the skink are due to large deletions in the T. rugosa genome. We also show that tuataras are on a growing list of species, including sharks, frogs, birds, alligators, and platypus, that can use an atypical TCR delta that appears to be a chimera of a TCR chain with an Ab-like Ag-binding domain. Tuatara represents the nearest living relative to squamates that retain gamma delta T cells. The loss of gamma delta TCR in the skink is due to genomic deletions that appear to be conserved in other squamates. The genes encoding the alpha beta TCR chains in the skink do not appear to have increased in complexity to compensate for the loss of gamma delta T cells.