Aging and longevity in the simplest animals and the quest for immortality

•Basal metazoans like sponges, jellyfish, corals and hydras often show great longevity and potential immortality.•These animals can have many pluripotent stem cells that maintain somatic cell lineages central to regeneration and rejuvenation.•These stem cell clones represent a holdover from immortal cell clones of single-celled organisms.•Early bilaterians such as flatworms often retain this system of stem cell-based immortality.•Higher bilaterians including humans have traded immortality for greater complexity and safeguards against unregulated cell growth.

Here we review the examples of great longevity and potential immortality in the earliest animal types and contrast and compare these to humans and other higher animals. We start by discussing aging in single-celled organisms such as yeast and ciliates, and the idea of the immortal cell clone. Then we describe how these cell clones could become organized into colonies of different cell types that lead to multicellular animal life. We survey aging and longevity in all of the basal metazoan groups including ctenophores (comb jellies), sponges, placozoans, cnidarians (hydras, jellyfish, corals and sea anemones) and myxozoans. Then we move to the simplest bilaterian animals (with a head, three body cell layers, and bilateral symmetry), the two phyla of flatworms. A key determinant of longevity and immortality in most of these simple animals is the large numbers of pluripotent stem cells that underlie the remarkable abilities of these animals to regenerate and rejuvenate themselves. Finally, we discuss briefly the evolution of the higher bilaterians and how longevity was reduced and immortality lost due to attainment of greater body complexity and cell cycle strategies that protect these complex organisms from developing tumors. We also briefly consider how the evolution of multiple aging-related mechanisms/pathways hinders our ability to understand and modify the aging process in higher organisms.