The findings, originally posted on bioRxiv*, provide new insight about natural selection, and help us understand how and why common multicellular life has evolved so many times on Earth.

Life on Earth has been transformed by the evolution of multicellular life forms. Multicellularity allowed organisms to develop specialised cells to carry out certain functions, such as being nerve cells, skin cells or muscle cells. It has long been assumed that this specialisation of cells will only occur when there are benefits. For example, if by specialising, cells can invest in two products A and B, then evolution will only favour specialisation if the total output of both A and B is greater than that produced by a generalist cell. However, to date, there is little evidence to support this concept.

"Rather than each cell producing what it needs, specialised cells need to be able to trade with each other. Previous work suggests that this only happens as long as the overall group's productivity keeps increasing," explains lead author David Yanni, PhD student at Georgia Institute of Technology, Atlanta, US. "Understanding the evolution of cell-to-cell trade requires us to know the extent of social interactions between cells, and this is dictated by the structure of the networks between them."

To study this further, the team used network theory to develop a mathematical model that allowed them to explore how different cell network characteristics affect the evolution of specialisation. They separated out two key measurements of cell group fitness -- viability (the cells' ability to survive) and fecundity (the cells' ability to reproduce). This is similar to how multicellular organisms divide labour in real life -- germ cells carry out reproduction and somatic cells work to ensure the organism survives.

In the model, cells can share some of the outputs of their investment in viability with other cells, but they cannot share outputs of efforts in reproduction. So, within a multicellular group, each cell's viability is the return on its own investment and that of others in the group, and gives an indication of the group's fitness.

By studying how the different network structures affected the group fitness, the team came to a surprising conclusion: they found that cell specialisation can be favoured even if this reduces the group's total productivity. In order to specialise, cells in the network must be sparsely connected, and they cannot share all the products of their labour equally. These match the conditions that are common in the early evolution of multicellular organisms -- where cells naturally share viability and reproduction tasks differently, often to the detriment of other cells in the group.

"Our results suggest that the evolution of complex multicellularity, indicated by the evolution of specialised cells, is simpler than previously thought, but only if a few certain criteria are met," concludes senior author Peter Yunker, Assistant Professor at Georgia Institute of Technology, Atlanta, US. "This contrasts directly to the prevailing view that increasing returns are required for natural selection to favour increased specialisation."

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Journal Reference:

1. David Yanni, Shane Jacobeen, Pedro Márquez-Zacarías, Joshua S Weitz, William C Ratcliff, Peter J Yunker. Topological constraints in early multicellularity favor reproductive division of labor. eLife, 2020; 9 DOI: 10.7554/eLife.54348