Allorecognition elements on a urochordate histocompatibility locus indicate unprecedented extensive polymorphism

Abstract

Tissue contacts between different colonies of the cosmopolitan urochordate Botryllus schlosseri resulted either in fusion between allogenic blood vessels or in the formation of rejections, characterized by necrotic areas. This colony specificity is manifested by a single, highly polymorphic mendelian locus, with codominantly expressed alleles, called the tunicate fusibility/histocompatibility (Fu/HC) haplotype. Two colonies sharing even one allele at the Fu/HC locus may fuse; rejecting colonies share no alleles. Previous studies have revealed up to 100 alleles on the Fu/HC locus in different natural populations. We studied Fu/HC polymorphism in three populations (> 1000 colonies) along the Mediterranean coast of Israel, 12-36 km apart. By using the protocol of colony allorecognition assays (CAAS) on 444 tests within localities, 58-306 alleles per locality were calculated. We also estimate a total of 479-560 Fu/HC alleles in the three Israeli populations. An additional 103 interpopulation CAAS resulted in zero fusion, an outcome which contradicts previous findings showing 4.4-12.0% fusions between more remote B. schlosseri populations such as those from Israel versus Monterey, California, and California versus Japan assays. We propose that the recorded unprecedented Fu/HC polymorphism is maintained through overdominant selection, which is promoted by the gregarious settlement of Fu/HC-compatible larvae and by the subsequent threat of germ cell parasitism following colony fusion.