Evolution of regulated phenotypic expression during a transition to multicellularity

Abstract

Multicellular organisms coordinate growth and differentiation from single cell starting points with developmental programs. While the evolutionary origins of these programs are unknown, it is likely that they are closely tied to the evolution of regulatednot stochastic-phenotypic expression. To determine how such regulation might arise, we consider experimental populations of Pseudomonas fluorescens which evolved stochastic switching in the lab. This switching is directly coupled with environmental oscillations generated by the bacteria themselves. This unique example of niche construction provides reliable information that organisms may incorporate into regulation of phenotypes. We use mathematical models to investigate the success of two forms of regulation that rely on sensing either external or internal information. We find that both strategies can outcompete stochastic strategies for certain combinations of parameters. In particular, external sensing mechanisms are very effective over a large range of parameter space-including parameters that correspond to poor sensing of the extracellular signal and gradual responses. We show with evolutionary simulations that this robustness makes them more likely to evolve from initially stochastically switching populations rather than internal sensing mechanisms which require more tuning of parameters. These results demonstrate that, within this oscillating system, if regulatory mechanisms can evolve to incorporate environmental information then their selective advantage is sufficient for them to fix in the population.

The Consequences of Budding versus Binary Fission on Adaptation and Aging in Primitive Multicellularity

“…Many of the major conceptual topics surrounding the evolution of multicellularity fall under this category. These include: (i) how multicellular groups form and become Darwinian units capable of adaptation [ 18 , 29 , 30 , 31 , 32 , 33 ], (ii) how the transition to multicellularity affects subsequent evolutionary processes [ 6 , 34 ], (iii) how cooperative behaviors associated with complex multicellular organisms (e.g., cellular differentiation) evolve and remain stable in the face of social defection [ 35 , 36 , 37 , 38 , 39 , 40 ], (iv) how multicellular life cycles arise and shape the subsequent evolution of multicellularity [ 13 , 14 , 41 ], and (v) how multicellular lineages co-opt and modify traits of their unicellular ancestor for novel multicellular purposes [ 21 , 27 , 42 , 43 , 44 ].…”

A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems

“…Niche construction theory also emphasizes (more so than eco‐evolutionary feedback) a role of inherited environments as a parallel route of inheritance (Danchin, ; Odling‐Smee et al ., ). Niche construction can also cause plastic phenotypic responses, thereby influencing phenotypic variation available for selection and the evolution of reaction norms (Badyaev & Uller, ; Donohue, ; Moczek, ; Sultan, ; Wolinsky & Libby, ; Hendry, ). Eco evo theory has, however, largely ignored the fact that phenotypic variation is shaped by ecological conditions through development and that developmental outcomes can reciprocally influence ecological conditions (e.g.…”

Aggregative cycles evolve as a solution to conflicts in social investment

“…The timing of these phases depends on cell-level parameters, and changes along the evolutionary trajectory. As in the case of extrinsic oscillations, such alternating selective pressures, generated by genetically distinct partners, may set the scene for selection of more complex strategies for cell behaviour, notably phenotypic switching [ 39 ] or context-dependent phenotype determination [ 15 , 16 , 40 ]. The possibility that extrinsically imposed periodic changes in selection lead to the emergence of phenotypic variation typically associated to life cycles has been experimentally demonstrated in Hammerschmidt et al [ 17 ].…”