Coexistence and Possible Parasitism of Somatic and Germ Cell Lines in Chimeras of the Colonial Urochordate Botryllus schlosseri

Abstract

Fusion between conspecifics (chimerism) is a well-documented phenomenon in a variety of taxa. Chimerism and the subsequent mixing of genetically different stem cell lines may lead to competition between cell lineages for positions in the germ line and to somatic and germ cell parasitism. It is suggested that somatic compatibility systems evolved to alleviate the costs and the threat of such cell lineage competition. Allogeneic colonies of the ascidian Botryllus schlosseri form vascular chimeras based on matching in one or both alleles on one highly polymorphic fusibility haplotype. Thereafter, one of the partners is completely or partially resorbed. Here we used a polymorphic molecular marker (PCR typing at a microsatellite locus) to follow somatic and gametic consequences of chimera formation. Twenty-two chimeras and subclone samples were established from 12 different genotype combinations, in which blood cells, zooids, and gonads were typed 45-130 days thereafter. Somatic coexistence of both partners was recorded in 73% of the subcloned chimeras (83% of chimeric entities) up to 100 days after disconnection between genotypes and in all chimeras where colony-resorption was completed. Both genotypes were present in 23% of the sampled gonads (in 33% of the chimeras), and in 22% of the cases, germ cells of the second partner only were detected. Injection of allogeneic but compatible blood cells into three recipient colonies revealed proliferation of the donor cells in one case, 100 days after injection. To further evaluate somatic and germ cell parasitism in chimeric organisms, we propose four key features that characterize cell lineage competition processes. These include the somatic embryogenesis mode of development, the capability for independent existence of stem cells, the disproportionate share of gametic output within chimeras, and the existence of hierarchial responses.