Division of labour and the evolution of multicellularity

Abstract

Understanding the emergence and evolution of multicellularity and cellular differentiation is a core problem in biology. We develop a quantitative model that shows that a multicellular form emerges from genetically identical unicellular ancestors when the compartmentalization of poorly compatible physiological processes into component cells of an aggregate produces a fitness advantage. This division of labour between the cells in the aggregate occurs spontaneously at the regulatory level owing to mechanisms present in unicellular ancestors and does not require any genetic predisposition for a particular role in the aggregate or any orchestrated cooperative behaviour of aggregate cells. Mathematically, aggregation implies an increase in the dimensionality of phenotype space that generates a fitness landscape with new fitness maxima, in which the unicellular states of optimized metabolism become fitness saddle points. Evolution of multicellularity is modelled as evolution of a hereditary parameter: the propensity of cells to stick together, which determines the fraction of time a cell spends in the aggregate form. Stickiness can increase evolutionarily owing to the fitness advantage generated by the division of labour between cells in an aggregate.

Figure 1.

(a) The metabolic fitness landscape for single cells (defined by equation (2.5)) and (b) for the corresponding two-cell aggregates (defined by equation (2.6)). For the two-cellular fitness, we have assumed an anti-symmetry between the metabolic states of the cells, x₁ = y₂ and x₂ = y₁. The form of the fitness landscape (equation (2.6)) implies that the maxima visible in (b) remain the same in the unrestricted four-dimensional space {x₁, y₁, x₂, y₂}. The figure shows how a maximum on the diagonal x = y in (a), corresponding to equal rates of production of x and y, becomes a saddle point for the two-cell fitness landscape in (b). Two maxima near the horizontal and vertical axes in panel (b) correspond to compartmentalization of production of x and y in the two-cell state: while one cell produces only x, the other cell produces only y. The white area in the plots corresponds to negative birth rates (i.e. B – C< 0). The landscapes shown correspond to c_x = c_y = c = 1/25.

Figure 2.

Evolution towards cell aggregation and two-cellularity. (a) The population distribution of the trait σ over time, with brighter areas indicating higher densities. (b) The proportion of two-cell aggregates, N₂/(N₁ + N₂), with N_j = ∫n_j(σ) dσ for j = 1,2 as a function of time. For the figure, equation (3.7) was solved numerically for the following parameters: k₊ = 10, k₋ = 1, δ = 1, M(x) = 1 − x/10 and D = 10⁻³. As mentioned earlier, the effective birth rates for unicellular and two-cellular forms were assumed to be perfectly optimized to the corresponding cellular state, R₁ = 0.866 and R₂ = 1.45.