The multicellular organisms and colonial superorganisms

Abstract Comparative data indicate that clades of differentiated multicellular organisms and colonial superorganisms always originated by somatic adherence to a diploid (zygotic) cell and by comparable loyalty of a worker caste to monogamous parents. However, the functional analogy remains ambiguous because multicellular animals ultimately die from somatic failure while single-queen colonies die from germline failure. This difference relates to the forms of corruption that plague the two levels of organizational complexity, metazoan cancers due to somatic mosaicicm and inquiline social parasites due to germline chimerism. Parental monogamy also shaped condition-dependent reproductive altruism in societies of cooperative breeders, which never became monogamous enough to evolve permanently altruistic castes. In addition to evidence for ultimate conjectures, I explore three proximate parallels between multicellular animals and colonial superorganisms. First, the ways in which germlines and soma segregate and differentiate in bodies and colonies; second, the principles by which superorganismal (but not society) immune defenses reached impressive efficiencies, particularly in ants and termites that defend non-overlapping territories; third, the extent of developmental similarity between cell differentiation in metazoan bodies and caste differentiation in superorganismal colonies. Early organismal biologists often appreciated these natural history parallels more than modern scientists, and even pre-Darwinian naturalists were remarkably competent observers of life’s organization. The empirical data appear consistent with expressions of condition-dependent somatic altruism by cells or multicellular individuals not being ancestral to obligate and unconditional reproductive altruism in (super)organismal clades. This challenges the reproductive bauplan concept for the origin of castes and suggests that the clarification of unique gene regulatory networks for obligate somatic altruism need to replace the reductionist identification of toolkit genes.