Rejection patterns in botryllid ascidian immunity: the first tier of allorecognition

Botryllid ascidians, a small but geographically widely distributed group of compound tunicates, are being used as a model system for the study of allorecognition. Botryllid ascidians possess a unique type of immunity. Pairs of colonies that meet through their extending ampullae either fuse to form a chimera or develop cytotoxic lesions at contact zones (rejection). This first tier of allorecognition is succeeded (in cases of fusion) by two additional tiers, not reviewed here (the colony resorption phenomenon and the phenomenon of somatic and germ cell parasitism). Fusion and rejection are controlled by a single highly polymorphic gene locus termed the fusibility/histocompatibility (Fu/HC) locus. One shared allele on the Fu/HC locus is enough for fusion. Rejecting colonies do not share any Fu/HC alleles. To date, 14 botryllid ascidians have been studied for their fusibility patterns; of these, the cosmopolitan species Botryllus schlosseri (Pallas, 1766) has emerged as the most studied taxon. This review summarizes studies revealing the various types of noncompatible responses that are expressed following the application of the colony allorecognition assay and the cut surface assay. These include divergent alloresponses related to different populations of the same botryllid species, distinctive allorecognition sites, polymorphism and a repertoire of Fu/HC alleles, a state of low responsiveness as opposed to the expected immunological memory, the retreat growth phenomenon, and the irreversible nature of the rejection process. A detailed description of the accumulated knowledge on the effector cells (morula cells and macrophages), the humoral and cellular molecules (at the biochemical and molecular levels), and the prophenoloxidase system is given. Links between allogeneic responses and the evolutionary ecology of botryllid ascidians are revealed. Since tunicates occupy a key phylogenetic position in the origin of the vertebrates, the study of colony allorecognition in this group may shed light on self/nonself recognition elements in other multicellular organisms, including vertebrates.