Bi-versus multichimerism in colonial urochordates: a hypothesis for links between natural tissue transplantation,...

Allogenic colonies of the cosmopolitan ascidian Botryllus schlosseri may fuse upon contact through their blood vessels to form chimeric entities if they share at least one allele at a highly polymorphic haplotype, termed the fusibility-histocompatibility (Fu/HC) locus. Past studies have attributed several benefits to this chimerism, but none of the suggestions was confirmed by controlled laboratory studies. Furthermore, once Botryllus colonies fuse, a second allorecognition phenomenon begins which usually leads to the resorption of one partner in the chimera. Resorption is probably controlled by a multilevel hierarchial organization of the heterozygosity relatedness for several allorecognition elements (the Fu/HC and resorption loci), which also reflects the relative heterozygosity of each partner's genome. Consequently, the more heterozygotic partner will be the 'winner' in the resorption, leaving alive the most adapted genotype (sensu to the heterosis concept). However, recent studies have recorded that freely circulating stem cells from the 'subordinate' partner in the resorption phenomenon may parasitize the 'winner' for positions on the germ line. All the above studies have been performed on bichimeric entities. It is suggested here that formation of natural multichimeras in this species (resulting from an aggregated cosettlement of Fu/HC compatible colonies) produces more 'equilibrated' chimeric entities and alleviates the costs incurred through the contradicting heterosis and germ cell parasitism processes. This improves the interspecific competitive ability of the multifusion entities. Therefore, in this case, selection acts on the 'group' level, not the colony level, providing the evolutionary forces that shape the phenomenon of natural tissue transplantation in these organisms.