In the 19th century, biologists came to appreciate for the first time the fundamentality of the cell to all life on Earth. One of the early pioneers of cell biology, Rudolf Virchow, realized that the discovery of this cell brought with it a new way of seeing the organism. In an 1859 essay he described the organism as a ‘cell state’, or Zellenstaat, a ”society of cells, a tiny, well-ordered state, with all of the accessories—high officials and underlings, servants and masters, the great and the small.” In the 20th century, the ‘cell state’ metaphor fell out of favour in biology, but three recent trends in biology suggest it is due a revival.

Firstly, there is our growing awareness of cooperation among microorganisms. Some social behaviours in microbes, such as the formation of fruiting bodies in social amoebas, result in phenomena that resemble simple multicellular organisms. Some authors have even suggested that bacterial biofilms should be regarded as organisms in their own right.

Secondly, in insect biology, there has been a revival of interest in the ‘superorganism’: the idea that we should think of an insect colony as a single organism. While this idea has always been controversial, even to consider it is to recognize the possibility that a high degree of social complexity can in principle give rise to a new, organism-like entity.

Finally, a research program called ‘major transition theory’ has led to a radical re-evaluation of the place of cooperation in the history of life. Building on foundations laid by Leo Buss, John Tyler Bonner, John Maynard Smith, and Eörs Szathmáry, major transitions researchers portray the history of life as a series of ‘evolutionary transitions in individuality’ in which integrated individuals have evolved, through social evolution, from groups of smaller entities.

When we look at evolution in this new light, we start to see social phenomena where we saw none before. We see cooperation among cells within multicellular organisms, among organelles within cells, even among genes within a chromosome. The result has been a dramatic increase in the ambitions of social evolution research—and the return of ‘cell state’ thinking.

Importantly, for social evolution theorists working on the origins of multicellular life, the ‘cell state’ is more than a metaphor. It’s the foundation for a research program. Taking a ‘social perspective’ on the organism does not simply mean describing the activities of cells in social terms. It means drawing on the concepts of social evolution theory to explain the origins of multicellular individuals.

Taking a ‘social perspective’ on the organism does not simply mean describing the activities of cells in social terms. It means drawing on the concepts of social evolution theory to explain the origins of multicellular individuals.

For one of the pioneers of major transition theory, Leo Buss, multicellular life presented the following puzzle: given that natural selection favours cells that promote their own reproduction, how did early multicellular organisms avoid being destabilized by conflict among cell lineages? His answer was that organisms have evolved, through group selection, mechanisms for controlling internal conflict, such as ‘germline segregation’, whereby the capacity to generate a new organism is limited to a very small number of cell lineages called the ‘germline’. This, however, led to a ‘chicken and egg’ puzzle. How could group selection be powerful enough to assemble such mechanisms prior to the existence of such mechanisms?

What Buss missed is that organisms are clonal groups—they are genetically identical—and the evolutionary interests of genetically identical individuals are perfectly aligned. This neutralizes the conflict. As W. D. Hamilton, creator of the theory of kin selection, observed in the 1960s:

“Our theory predicts for clones a complete absence of any form of competition which is not to the overall advantage and also the highest degree of mutual altruism. This is borne out well enough by the behavior of clones which make up the bodies of multicellular organisms.”

In other words, the cells of multicellular organisms cooperate because they are genetically identical. Let’s call this ‘Hamilton’s hypothesis.’

Hamilton’s hypothesis is complicated by the fact that few organisms are fully clonal. Clonality is a feature of organisms that develop from a single cell, but not all development is like this. For example, many plants can reproduce vegetatively, with the new individual developing from a multicellular offshoot.

In plants under cultivation, generations of vegetative reproduction lead to the accumulation of mutations in different cell layers, resulting in individuals containing internal genetic diversity. In the wild, however, plants frequently reproduce sexually, pushing their lineage through a single-cell bottleneck and restoring high relatedness. Provided this happens often enough, high genetic relatedness and low internal conflict can be maintained.

Even among organisms that pass through a single-cell bottleneck every generation, such as multicellular animals, clonality is not perfect. Within-organism genetic diversity can arise through ‘chimerism’, where cell lineages produced from a different sperm and egg mix in the early stages of development. We see this, for example, in marmosets.

Genetic diversity also arises through mutation. Sometimes, mutation events lead to cancer, and the survival of the population relies on these cancerous ‘cheater’ lineages being unable to spread between organisms. We see a grim illustration of this point in the Tasmanian devil, now threatened with extinction due to an epidemic of facial tumours. Given this, we should not be surprised to find that an ability to discriminate ‘self’ from ‘non-self’, and to attack intruding cell lineages, is present even in sponges, often regarded as among the most simple multicellular animals.

Yet for all these caveats, it remains plausible that, for any organism spawned from a single cell, genetic relatedness is high enough to stabilize cooperation among the cells. It’s also plausible that organisms which can reproduce vegetatively pass through a single-cell bottleneck often enough to maintain high relatedness. So it seems like Hamilton’s insight has stood the test of time—as has Virchow’s. The organism began as a cooperative enterprise between independently viable cells. Those cells cooperated—and, hundreds of millions of years later, still cooperate—because they are genetic relatives.

Featured image credit: Dictyostelium discoideum 43 by Usman Bashir. CC-BY-SA-4.0 via Wikimedia Commons.