Phenotypic plasticity, life cycles, and the evolutionary transition to multicellularity

Abstract

Understanding the evolutionary transition to multicellularity is a key problem in evolutionary biology (1,2). While around 25 independent instances of the evolution of multicellular existence are known across the tree of life (3), the ecological conditions that drive such transformations are not well understood. The first known transition to multicellularity occurred approximately 2.5 billion years ago in cyanobacteria (4,5,6), and today's cyanobacteria are characterized by an enormous morphological diversity, ranging from single-celled species over simple filamentous to highly differentiated filamentous ones (7,8). While the cyanobacterium Cyanothece sp. ATCC 51142 was isolated from the intertidal zone of the U.S. Gulf Coast as a unicellular species (9), we are first to additionally report a phenotypically mixed strategy where multicellular filaments and unicellular stages alternate. We experimentally demonstrate that the facultative multicellular life cycle depends on environmental conditions, such as salinity and population density, and use a theoretical model to explore the process of filament dissolution. While results predict that the observed response can be caused by an excreted compound in the medium, we cannot fully exclude changes in nutrient availability (as in (10,11)). The best fit modeling results demonstrate a nonlinear effect of the compound, which is characteristic for density-dependent sensing systems (12,13). Further, filament fragmentation is predicted to occur by means of connection cleavage rather than by cell death of every alternate cell. The phenotypic switch between the single-celled and multicellular morphology constitutes an environmentally dependent life cycle, which likely represents an important step en route to permanent multicellularity.

Tradeoff breaking as a model of evolutionary transitions in individuality and limits of the fitness-decoupling metaphor

“…Before an ETI starts, the unicellular ancestors have been selected for traits that optimise growth rate in a unicellular environment under the constraints of their genetic constitution (‘Tradeoff-optimal particle phenotype’; blue disk in Figure 8 ). Then, a mutation (e.g., loss of the transcription factor ACE2, resulting in snowflake-shaped yeast clusters; see Ratcliff et al, 2015 ), a plastic change in phenotype (e.g., filament formation under low population densities in cyanobacteria; see Tang et al, 2022 ), a change in the structure of the environment (as in the ecological scaffolding model for the origin of multicellularity; see Black et al, 2020 ), or even a combination of several factors (‘wrinkly spreader’ mats arising by mutation and ecological scaffolding; see Hammerschmidt et al, 2014 ) promote the formation of collectives ( Figure 8 ). Multicellular collectives define a new environment where the optimal trait values are potentially different.…”

Tradeoff breaking as model of evolutionary transitions in individuality and the limits of the fitness decoupling metaphor

“…Before an ETI starts, the unicellular ancestors have been selected for traits that optimise growth rate in a unicellular environment under the constraints of their genetic constitution ("Tradeoff-Optimal particle phenotype"; blue disk in Figure 8). Then, a mutation (e.g., loss of the transcription factor ACE2, resulting in snowflake-shaped yeast clusters, Ratcliff et al, 2015), a plastic change in phenotype (e.g., filament formation under low population densities in cyanobacteria, Tang et al, 2021), a change in the structure of the environment (as in the ecological scaffolding model for the origin of multicellularity, Black et al, 2020) or even a combination of several factors ("wrinkly spreader" (WS) mats arising by mutation and ecological scaffolding, Hammerschmidt et al, 2014) promote the formation of collectives (Figure 8). Multicellular collectives define a new environment where the optimal trait values are potentially different.…”

Bacteria evolve macroscopic multicellularity via the canalization of phenotypically plastic cell clustering

“…For example, phytoplankton 28 , cyanobacteria 29 , and Pseudomonads 30,31 can facultatively form multicellular clusters in response to predation. Moreover, a recent study has shown that changes in environmental salinity can induce multicellular clustering in marine cyanobacteria 32 . Such prevalence of facultative cell clustering across diverse unicellular taxa suggests that phenotypic plasticity may be an important force in the evolution of multicellularity.…”