A Colonial Invertebrate Species that Displays a Hierarchy of Allorecognition Responses

When two colonies of the compound ascidian Botryllus schlosseri come into contact with each other, they either fuse or reject. This allorecognition is governed genetically by multiple, codominantly expressed alleles at a single, highly polymorphic haplotype called the fusibility/histocompatibility (Fu/HC) locus. Two colonies sharing one or both alleles at this locus can fuse via their extracorporeal tunic blood vessels. Thereafter, in laboratory studies, one partner in the chimera is usually resorbed. The direction of resorption appears to be inherited, as multiple subclones of asexually-derived individuals from colony A always resorb paired subclones from colony B, independent of laboratory conditions or colony age. We established 121 pairs of chimeric partners by fusions of relatives from four generations within a pedigree, all homozygotes (AA line) at their Fu/HC haplotype. This was carried out by self- and defined-crosses done in the laboratory on two outbred founder colonies (each AB at the fusibility locus) which were taken from the field. We found that the resorption phenomenon is characterized by a linear hierarchy within each generation of colonies, which is expressed by the existence of at least 5 intermediate groups. However, the time for resorption did not correlate with the position in the hierarchy. Analysis of resorption hierarchies between different generations revealed that mother colonies always resorbed their self crossed offspring. More interesting, colonies low in the hierarchy within a specific generation reproducibly resorbed the self crossed offspring of a superior kin. Chimeras between defined-crossed offspring of different generations revealed nontransitive types of hierarchies which were correlated with the relative position of each colony in the linear hierarchy established for the colonies within each generation. We propose that colony resorption in colonial botryllid ascidians is controlled by several allorecognition elements that determine a resorption hierarchy.