Selection by somatic signals: the advertisement of phenotypic state through costly intercellular signals

Abstract

We develop a model of intercellular signalling, to explore the possibility that the signals exchanged between cells within a body may be subject to many of the same evolutionary pressures as signals exchanged between individuals whose genetic interests conflict. Evolutionary signalling theory maintains that signals, to be reliable indicators of need, intention or quality must be more costly than would be required merely to transmit a message. Cost guarantees that poor quality individuals are less able to display the high magnitude signals produced by the higher quality individuals. Receivers have been favoured by natural selection to attend only to the costliest signals, and thereby acquire honest information from the signaller. Hence the extravagant, costly ornamentation found among males of many species, ensures that females can accurately choose among them on the basis of their qualities. However, because somatic cells are normally perfectly genetically related, and are often denied access to the germ line, there will be minimal genetic conflicts of interest. This appears to imply that reliable intercellular signals should be produced without the need for cost to ensure their reliability. Nevertheless, we show that whenever cells vary in their phenotypic qualities in ways relevant to the fitness of the body, and given that there exists a class of cell that remains ‘ignorant’ of its phenotypic state, costly intercellular signalling will evolve as a form of quality control. Specifically, we show that given variation in the cell population, signal cost will aid the identification and removal of cells that over-represent their true phenotypic state, and which therefore could lower fitness. Cells that under-represent their state are simply outcompeted by other cells. The cells of a body employ signals in a variety of intercellular interactions, including the development of the nervous system, the formation of neuromuscular junctions, and during the establishment of the immune repetoire. In each of these cases, cells may employ costly signals to advertise their phenotypic quality to other cells, and we review the evidence in support of this hypothesis: in effect, the cells may possess a molecular counterpart to the peacock’s tail.