Certain nonclassical MHC class Ib molecules (class Ib) play critical roles in the differentiation and function of distinct subsets of invariant (i)T-cells expressing a semi-invariant T-cell receptor (TCR) repertoire. Although iT-cells are attracting attention because of their potential as specialized regulators of immune function, the full biological significance and evolutionary ancestry of iT cells and their restricting class Ib molecules is just starting to emerge. Unlike mammals that possess few unambiguous class Ib gene orthologs, two divergent amphibian species Xenopus laevis and X. tropicalis (~ 65 million years), exhibit multiple class Ib gene lineages unusually conserved in a large cluster containing more than 20 Xenopus non-classical (XNCs) genes located outside the MHC locus. Some XNC gene lineages display flexibility with species-specific expansion or contractions, whereas other lineages have remained oligogenic with minimal intra-species sequence variations. Notably, six of these oligogenic XNC genes are expressed preferentially by X. laevis tadpole thymocytes at higher level than adults, whereas consistent thymic expression of classical MHC class Ia protein occurs only in adult. Furthermore, a corresponding 6 distinct TCRa rearrangements dominate (75%) the tadpoles TCRa repertoire. This suggests a preponderant role of several XNC-restricted iT-cell populations in X. laevis tadpoles when classical MHC class Ia function is suboptimal. Functional analysis using the ecologically relevant amphibian ranavirus pathogen FV3 in combination with XNC-tetramers and RNAi loss-of-function by transgenesis has revealed that the oligogenic XNC10 is required for the development of a distinct iT cell subset (iVα6 T-cells) reminiscent of mammalian iNKT-cells. These iVα6 T cells critically promote antiviral and anti-tumor immunity as well as antimicrobial macrophage effector functions. Preliminary study suggests that a gut-associated XNC-restricted iT-cell subset is also present in X. laevis. Our work provides strong evolutionarily-based support of the importance of class Ib-restricted iT-cells in vertebrates immunity.