Colony specificity in the colonial tunicate botryllus and the origins of vertebrate immunity

SYNOPSIS. Colonies of the compound tunicate Botryllus show the capacity for self-nonself discrimination by fusion between separated pieces of the same colony and rejection between pieces of unrelated colonies. We have found that genes controlling this colony specificity are similar to those which cause transplant rejection in the vertebrates. Like the loci within the vertebrate major histocompatibility complex (MHC), Botryllus fusibility (or histocompatibility) genes are highly polymorphic. In Botryllus, the histocompatibility complex also controls self-sterility, and limits cross-fertilization between colonies sharing histocompatibility alleles. The mouse MHC, the H-2 region, is linked to loci which also affect the frequencies of alleles at H-2 loci in mouse populations. Thus both systems contain characters which could act to promote the heterozygous condition at the linked histocompatibility loci. We suggest that such linked characters are responsible for the evolution of allogeneic polymorphism in vertebrates (however currently maintained), and that tunicate fusibility loci may be the evolutionary precursors of vertebrate MHC genes.