Stuart A. Newman

The origination and evolution of multicellular form and function is generally thought to be based on gene-based variation, with natural selection changing the populational composition in the respective variants over time. The criterion for evolutionary success is differential fitness, the relative capacity to leave progeny in the next generation. Theoretical considerations show that this model implies that phenotypic evolution will generally be gradual, based on variations of small effect. But the fossil record of early phylogenesis, notably for the metazoans, or animals, does not support the gradualist scenario. Moreover, discordances of phenotype and genotype in extant species, along with the existence of a pan-metazoan developmental genetic toolkit, does not support the gene-variation-based evolutionary mechanism, at least at the level of phyla. Most importantly, all life-forms, including the cells that constitute animal embryos, exhibit agency, and associations of cells (even constructed ones with no history of natural selection) exhibit novel kinds of agency. This strongly suggests that new multicellular forms can invent new ways of life (e.g., ecological niches) and can persist without supplanting their populational cohorts. This chapter describes how anatomical (e.g., segments, appendages) and functional (e.g., muscle, nerve) phenotypes can emerge without cycles of gradual selection from inherent properties of metazoan cells and their aggregates. While such phenotypic “add-ons” could provide enablements for exploration of new niches, it is implausible that they arose as adaptations to external challenges. Reproductive fitness, which is essential for understanding biogeography and ecology, is unlikely to have played a role in phylum-level evolution.