The Origin of Multicellularity

What I offer in this essay departs from my usual rule of confining myself to subjects in with I have personal research experience. It is a zoologist’s view of a complex matter.

The transition from single cell organism to multicellular ones like ourselves involves  the emergence of an entirely novel kind of life (Maynard Smith and Szathmary, 2010). This is Richard Dawkins' Threshold 4 (Dawkins, 1995). Such a major evolutionary transition brings with it interesting conceptual and evolutionary difficulties. A single cell that produces daughters by the usual method of splitting can readily be understood to lead to a colony if daughter cells stay together. Three evolutionary challenges emerge from the transition to such a colony. First, if they are to stay together, the selfish single cell parent is required to produce cooperative daughters.   Second, how is such a colony to reproduce?  Third, how is a colony to maintain integrity in the face of inevitable emergence of cheats which represent a return to the single cell selfish mode.

Fitness benefits for the cells in a colony flow from the shared protection of a soma  (body) – ‘the vehicle’ of Richard Dawkins (Dawkins, 1982). Costs include colony losses in fitness due to the emergence of cheats. It is often assumed that the emergence of cheats can be circumvented by unexplained adaptive mechanisms arising in the colony to suppress cheats. An alternative, seemingly less likely idea, is that cheats act as a germ line that facilitates colony reproduction, thus solving the second difficulty above (Hammerschmidt, Rose, Kerr, and Rainey, 2014) (Fig. 1.). Cheats as a novel germ line (gametes), open up an unprecedented adaptive world. An example that illustrates this model is Volvox (Fig. 2).

Fig. 1. A life cycle of a simple organism switching between the singe cell ancestor (a), and a colony of co-operative daughters (b). In (c), a mutant cheat has arisen which escapes (d), and reproduces a mix of cooperatives and cheats (pink).

Fig. 2.  The eukaryote cell Volvox (c. 0.25mm diameter), with cells of spherical soma enclosing germ cells. Two of these are shaded pink to show analogy to the cheats in Fig. 1c. (Modified from the internet).

The idea that cheat cells originate as specialised reproductive cells has been tested in an extraordinary series of experiments by Paul Rainey and colleagues using the bacterium Pseudomonas fluorescens as the test organism. If I understand them correctly, they view the embracing of cheats as an innovation that has lead to an adaptive radiation of organisms both large and complex.

It is instructive to note that in this essay I have adopted a cell division model for the origin of multicellularity. But this is not the only origin possible. The little known but extraordinary creatures called slime moulds achieve multicellularity, not by cell division as in  Volvox, but instead by cell aggregation. Single cell, free living amoebae aggregate to form complex, often strikingly beautiful complex organisms. To illustrate this I have added two pictures of slime moulds from the internet.  John Tyler Bonner has spent much of his professional life in the study of  slime moulds and his book entitled Life Cycles (1993), is well worth a read. 

Whatever the method of achieving multicellarity, the time has come to substitute the term ‘cancer’ for ‘cheats’. Cancer has a presence in our human consciousness as a much feared disease. It appears to involve the regression of cooperative body cells to an original selfish single cell state accompanied by uncontrolled proliferation to create a tumour (Nowell, 1976). A tumour, I suggest is the adaptive equivalent of the ancestral colony. The adaptive battle between cooperatives and cheats takes place in the tumour. In this view, cost to the organism  as a whole would seem incidental. Note there are here two somas, the phenotype and the smaller cancer tumour. 

To summarise; as we know the original emergence of cancer cells in the evolutionary transition to multicellularity does not exclude its re-emergence as a disease. Indeed the emergence of cheats of many kinds, in colonies as we have seen but also in the behaviour of metazoa (multicellular animals), such as that based on reciprocal altruism or frequency dependent selection (Davies, Krebs, and West, 2012), and indeed wherever there is co-operation. It may be said that the incorporation of a cheating strategy to our understanding of evolution underlies many of the revelations of neo-Darwinism. For a different approach to the origin of multicellularity see Bonner (1978).

references
Bonner, J. T. (1993). Life Cycles. Reflections of an evolutionary biologist. Princeton University Press. Princeton, New Jersey. 

Bonner, J. T. (1978). On Development. The Biology of Form. Harvard University Press. 

Davies, N. B., Krebs, J. R., and West, S. A. (2012). An Introduction to Behavioural Ecology. (4 ed.). Oxford: Wiley-Blackwell.

Dawkins, R. (1982). The Extended Phenotype. (1999 edition ed.). Oxford: Oxford University Press.
Dawkins, R. (1996). Climbing mount improbable. W. H. Norton & Co, London.
Dawkins, R. (1995). River Out of Eden. Phoenix, London.

Hammerschmidt, K., Rose, C. J., Kerr, B., and Rainey, P. B. (2014). Life Cycles, Fitness Decoupling and the Evolution of Multicellularity. . Nature, 515, 75 - 79.

Maynard Smith, J., and Szathmary, E. (2010). The Major Transitions in Evolution. Oxford: Oxford University Press.

Nowell, C. P. (1976). The clonal evolution of tumour cell populations. Science, 194, 23-28.