A food's-eye view of the transition from basal metazoans to bilaterians

Abstract

Living things invariably consist of some kind of compartmentalized redox chemistry. Signaling pathways mediated by oxidation and reduction thus derive from the nature of life itself. The role of such redox or metabolic signaling broadened with major transitions in the history of life. Prokaryotes often use redox signals to deploy one or more variant electron carriers and associated enzymes to better utilize environmental energy sources. Eukaryotes transcend the strong surface-to-volume constraints inherent in prokaryotic cells by moving chemiosmotic membranes internally. As a consequence, eukaryotic redox signaling is frequently between these organelle membranes and the nucleus, thus potentially involving levels-of-selection synergies and antagonisms. Gradients of oxygen and substrate in simple multicellular organisms similarly associated metabolic signaling with levels of selection, now at the level of the cell and the organism. By allowing sequestration of large amounts of food, the evolution of the animal mouth was a pivotal event in metabolic signaling, leading to "multicellular" redox regulation. Because concentrated food resources may be patchy in time and space, long-lived sedentary animals with mouths employ such metabolic signaling and phenotypic plasticity in ways that adapt them to the changing availability of food. Alternatively, if the mouth is coupled to a battery of sensory equipment, the organism can actively seek out and sequester patches of food. In these early bilaterians, competition for food resources may have favored rapid development with little subsequent plasticity and metabolic signaling. With rapid dispersal and colonization, such "assembly-line" animals could effectively compete for patchy resources. Limiting metabolic signaling, however, resulted in a cascade of seemingly unrelated changes. These changes derive from the effectiveness of metabolic signaling in policing variation at the cellular level. If the signals an organism uses to control cellular replication are the same as the signals a cell uses to control its own metabolism, then cells that ignore these signals and carry out selfish replication will pay a fitness cost in terms of inefficient metabolism. Bilaterians with limited metabolic signaling thus require other mechanisms to police cell-level variation. Bilaterian features such as restricted somatic cell potency, a sequestered germ line, and determinate growth should be viewed in this context. Bilaterian senescence evolved as a by-product of restricted potency of somatic cells, itself a mechanism of cell policing required by limited metabolic signaling.