Geometry shapes evolution of early multicellularity

Abstract

Organisms have increased in complexity through a series of major evolutionary transitions, in which formerly autonomous entities become parts of a novel higher-level entity. One intriguing feature of the higher-level entity after some major transitions is a division of reproductive labor among its lower-level units in which reproduction is the sole responsibility of a subset of units. Although it can have clear benefits once established, it is unknown how such reproductive division of labor originates. We consider a recent evolution experiment on the yeast Saccharomyces cerevisiae as a unique platform to address the issue of reproductive differentiation during an evolutionary transition in individuality. In the experiment, independent yeast lineages evolved a multicellular ''snowflake-like'' cluster formed in response to gravity selection. Shortly after the evolution of clusters, the yeast evolved higher rates of cell death. While cell death enables clusters to split apart and form new groups, it also reduces their performance in the face of gravity selection. To understand the selective value of increased cell death, we create a mathematical model of the cellular arrangement within snowflake yeast clusters. The model reveals that the mechanism of cell death and the geometry of the snowflake interact in complex, evolutionarily important ways. We find that the organization of snowflake yeast imposes powerful limitations on the available space for new cell growth. By dying more frequently, cells in clusters avoid encountering space limitations, and, paradoxically, reach higher numbers. In addition, selection for particular group sizes can explain the increased rate of apoptosis both in terms of total cell number and total numbers of collectives. Thus, by considering the geometry of a primitive multicellular organism we can gain insight into the initial emergence of reproductive division of labor during an evolutionary transition in individuality.

Experimental evolution reveals favored adaptive routes to cell aggregation in yeast

“…These results are consistent with prior literature showing that loss-of-function mutations in this gene cause settling/clumping phenotypes in other experimental evolution scenarios (Voth et al 2005;Koschwanez et al 2013;Oud et al 2013;Ratcliff et al 2015). Furthermore, ace2 null mutants have the characteristic cell separation defect that we observed in our clones (Libby et al 2014;Ratcliff et al 2015). Using complementation with the wild-type allele, we verified that the ACE2 mutations were causative of the separation defect aggregation phenotype in these two clones (Table 1), with subtle modification to the cell morphology by BEM2-a gene involved in bud emergence that is also mutated in both clones ( Figure S2B in File S1) (Bender and Pringle 1991;Kim et al 1994).…”

Cellular packing, mechanical stress and the evolution of multicellularity

“…Previous studies demonstrated that the elastic modulus of individual yeast cells is relatively constant with respect to cell size 16 ; if individual snowflake yeast cells behave similarly, the compressive modulus may be expected to increase if interior volume fraction increases 17,18 . It is important to note that the distribution of cells within clusters is very heterogeneous 7,19 ; cells in the cluster interior are much more crowded than those at the periphery (Fig. 1b,d).…”

Apoptosis in snowflake yeast: novel trait, or side effect of toxic waste?

“…Indeed, this mechanism should be considered a viable hypothesis to be tested in future experiments examining novel experimental lineages. More generally, nascent multicellular organisms are expected to be heavily affected by physical effects arising from their spatial structure [3,5,22,23]. Within-cluster gradients of nutrients, waste products and even previously evolved signalling molecules (e.g.…”

“…We modelled this effect quantitatively. The structure of a snowflake yeast cluster can be represented as a graph with a tree-like structure, in which cells are nodes and cell-cell connections are edges (figure 3a; [3,5]). Clusters reproduce when an edge is severed.…”

“…Production of proportionally smaller propagules is adaptive as long as their faster growth more than compensates for their reduced survival during settling selection at the end of the 24 h culture cycle. Indeed, evolutionary simulations show that this criterion is often met, as elevated apoptosis readily evolves in silico [4,5]. The distinction between these hypotheses is of crucial importance for properly interpreting Ratcliff et al's [2] experimental results: if elevated apoptosis is an adaptation to large size, not its side effect, it demonstrates that selection can readily favour the evolution of altruistic cellular traits in simple clusters of cells.…”