Cell polarity: having and making sense of direction—on the evolutionary significance of the primary cilium/centrosome organ in Metazoa

Abstract

Cell-autonomous polarity in Metazoans is evolutionarily conserved. I assume that permanent polarity in unicellular eukaryotes is required for cell motion and sensory reception, integration of these two activities being an evolutionarily constrained function. Metazoans are unique in making cohesive multicellular organisms through complete cell divisions. They evolved a primary cilium/centrosome (PC/C) organ, ensuring similar functions to the basal body/flagellum of unicellular eukaryotes, but in different cells, or in the same cell at different moments. The possibility that this innovation contributed to the evolution of individuality, in being instrumental in the early specification of the germ line during development, is further discussed. Then, using the example of highly regenerative organisms like planarians, which have lost PC/C organ in dividing cells, I discuss the possibility that part of the remodelling necessary to reach a new higher-level unit of selection in multi-cellular organisms has been triggered by conflicts among individual cell polarities to reach an organismic polarity. Finally, I briefly consider organisms with a sensorimotor organ like the brain that requires exceedingly elongated polarized cells for its activity. I conclude that beyond critical consequences for embryo development, the conservation of cell-autonomous polarity in Metazoans had far-reaching implications for the evolution of individuality.