The phenomenon of intraspecific germ cell parasitism may reveal a theoretical puzzle to the concept of Darwinian selection. In natural chimeras of the colonial protochordate Botryllus schlosseri, parasitic germ lines hitchhike with positively selected allogeneic soma, passing throughout successive generations without being visible to natural selection forces. This may cause the possible development of super-parasitic entities, specialized in allogeneic invasion and germ cell parasitism. Three evolutionary selected mechanisms (diversification of fusibility allele repertoire, the establishment of multichimeric entities, induction of programmed life spans) reduce opportunities for parasitic forms to hitchhike to a high frequency with selected genotypes, and may shape, on the other hand, more benign germ cell parasitic forms that share overlapping future expectations with their hosts. These benign forms are expected to contribute cells for somatic functions, forming entities with fitness that depends on joint genomic fitness of the partners. Population-level feedback thus may stabilize chimeric entities, shaping the evolution of chimerism.