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Regulatory mechanisms link phenotypic plasticity to evolvability.

van Gestel J, Weissing FJ - Sci Rep (2016)

Bottom Line: Using individual-based simulations, we compare the RN and GRN approach and find a number of striking differences.Most importantly, the GRN model results in a much higher diversity of responsive strategies than the RN model.The regulatory mechanisms that control plasticity therefore critically link phenotypic plasticity to the adaptive potential of biological populations.

View Article: PubMed Central - PubMed

Affiliation: Groningen Institute for Evolutionary Life Sciences, University of Groningen, P.O. Box 11103, Groningen 9700 CC, The Netherlands.

ABSTRACT
Organisms have a remarkable capacity to respond to environmental change. They can either respond directly, by means of phenotypic plasticity, or they can slowly adapt through evolution. Yet, how phenotypic plasticity links to evolutionary adaptability is largely unknown. Current studies of plasticity tend to adopt a phenomenological reaction norm (RN) approach, which neglects the mechanisms underlying plasticity. Focusing on a concrete question - the optimal timing of bacterial sporulation - we here also consider a mechanistic approach, the evolution of a gene regulatory network (GRN) underlying plasticity. Using individual-based simulations, we compare the RN and GRN approach and find a number of striking differences. Most importantly, the GRN model results in a much higher diversity of responsive strategies than the RN model. We show that each of the evolved strategies is pre-adapted to a unique set of unseen environmental conditions. The regulatory mechanisms that control plasticity therefore critically link phenotypic plasticity to the adaptive potential of biological populations.

No MeSH data available.


Related in: MedlinePlus

Colony growth and cell behaviours.(a) Individuals divide and differentiate on a two dimensional grid (blue, cells; red, spores). Cells sense the local environmental conditions, determined by the quadrant on which a cell is placed. Nutrients (green) and signal (not shown) diffuse in space. Colony growth occurs for a fixed number of time steps, after which all individuals can disperse. Spores are ten times more likely to survive dispersal than cells. (b) Cells can express three behaviours: (b1) cells can consume nutrients, which are converted to energy, and secrete molecular products in the local environment (called ‘signal’); (b2) cells with sufficient energy have a fixed probability to divide; (b3) cells can sporulate, which requires time and energy. Only cells that finish the sporulation process are more likely to survive dispersal than cells.
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f1: Colony growth and cell behaviours.(a) Individuals divide and differentiate on a two dimensional grid (blue, cells; red, spores). Cells sense the local environmental conditions, determined by the quadrant on which a cell is placed. Nutrients (green) and signal (not shown) diffuse in space. Colony growth occurs for a fixed number of time steps, after which all individuals can disperse. Spores are ten times more likely to survive dispersal than cells. (b) Cells can express three behaviours: (b1) cells can consume nutrients, which are converted to energy, and secrete molecular products in the local environment (called ‘signal’); (b2) cells with sufficient energy have a fixed probability to divide; (b3) cells can sporulate, which requires time and energy. Only cells that finish the sporulation process are more likely to survive dispersal than cells.

Mentions: We model a population of cells that grow inside a colony. The colony is placed on a two-dimensional surface that contains nutrients (Fig. 1a). Cells consume these nutrients, convert them to energy, and subsequently use this energy to divide. Hence, while colony growth progresses, nutrients get depleted. The colony grows for a fixed time period. At the end, cells can disperse and colonize a new nutrient surface, which forms the beginning of a new cycle of colony growth. We assume that cells only interact with their local environment. Thus, cells only consume nutrients from the grid element on which they are placed (see Material and Methods). These consumed nutrients are partly replenished by diffusion. We also assume that cells secrete a product into their local environment, which they can sense as well (Fig. 1b). We do not specify the nature of this product, so it can be anything from a waste product to a quorum-sensing signal. Take for example the soil bacterium Bacillus subtilis, it secretes numerous products during colony growth, these range from antimicrobials (e.g. surfactin)22 to pentapeptides (e.g. PhrC)231424. Even though these molecules might not primarily function as communicative signals, they are secreted and sensed by the cells and can affect the timing of sporulation1825. Henceforth we will refer to the secreted product in our model as ‘signal’. During colony growth, cells can decide to allocate their energy to cell division or sporulation (Fig. 1b). Sporulation requires time and energy and at end of sporulation a cell transforms into a spore. Spores are metabolically inactive and cannot divide, yet spores are ten times more likely to survive dispersal than cells. Thus, there is a trade-off between cell division and survival. The fitness of a genotype is largely determined by the number of spores it produces by the end of colony growth, which – as explained above – depends on the timing of sporulation. In fact, spore production forms an accurate proxy of fitness (Supplementary Fig. S1), even though cell production also contributes weakly to the reproductive success of a colony.


Regulatory mechanisms link phenotypic plasticity to evolvability.

van Gestel J, Weissing FJ - Sci Rep (2016)

Colony growth and cell behaviours.(a) Individuals divide and differentiate on a two dimensional grid (blue, cells; red, spores). Cells sense the local environmental conditions, determined by the quadrant on which a cell is placed. Nutrients (green) and signal (not shown) diffuse in space. Colony growth occurs for a fixed number of time steps, after which all individuals can disperse. Spores are ten times more likely to survive dispersal than cells. (b) Cells can express three behaviours: (b1) cells can consume nutrients, which are converted to energy, and secrete molecular products in the local environment (called ‘signal’); (b2) cells with sufficient energy have a fixed probability to divide; (b3) cells can sporulate, which requires time and energy. Only cells that finish the sporulation process are more likely to survive dispersal than cells.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4834480&req=5

f1: Colony growth and cell behaviours.(a) Individuals divide and differentiate on a two dimensional grid (blue, cells; red, spores). Cells sense the local environmental conditions, determined by the quadrant on which a cell is placed. Nutrients (green) and signal (not shown) diffuse in space. Colony growth occurs for a fixed number of time steps, after which all individuals can disperse. Spores are ten times more likely to survive dispersal than cells. (b) Cells can express three behaviours: (b1) cells can consume nutrients, which are converted to energy, and secrete molecular products in the local environment (called ‘signal’); (b2) cells with sufficient energy have a fixed probability to divide; (b3) cells can sporulate, which requires time and energy. Only cells that finish the sporulation process are more likely to survive dispersal than cells.
Mentions: We model a population of cells that grow inside a colony. The colony is placed on a two-dimensional surface that contains nutrients (Fig. 1a). Cells consume these nutrients, convert them to energy, and subsequently use this energy to divide. Hence, while colony growth progresses, nutrients get depleted. The colony grows for a fixed time period. At the end, cells can disperse and colonize a new nutrient surface, which forms the beginning of a new cycle of colony growth. We assume that cells only interact with their local environment. Thus, cells only consume nutrients from the grid element on which they are placed (see Material and Methods). These consumed nutrients are partly replenished by diffusion. We also assume that cells secrete a product into their local environment, which they can sense as well (Fig. 1b). We do not specify the nature of this product, so it can be anything from a waste product to a quorum-sensing signal. Take for example the soil bacterium Bacillus subtilis, it secretes numerous products during colony growth, these range from antimicrobials (e.g. surfactin)22 to pentapeptides (e.g. PhrC)231424. Even though these molecules might not primarily function as communicative signals, they are secreted and sensed by the cells and can affect the timing of sporulation1825. Henceforth we will refer to the secreted product in our model as ‘signal’. During colony growth, cells can decide to allocate their energy to cell division or sporulation (Fig. 1b). Sporulation requires time and energy and at end of sporulation a cell transforms into a spore. Spores are metabolically inactive and cannot divide, yet spores are ten times more likely to survive dispersal than cells. Thus, there is a trade-off between cell division and survival. The fitness of a genotype is largely determined by the number of spores it produces by the end of colony growth, which – as explained above – depends on the timing of sporulation. In fact, spore production forms an accurate proxy of fitness (Supplementary Fig. S1), even though cell production also contributes weakly to the reproductive success of a colony.

Bottom Line: Using individual-based simulations, we compare the RN and GRN approach and find a number of striking differences.Most importantly, the GRN model results in a much higher diversity of responsive strategies than the RN model.The regulatory mechanisms that control plasticity therefore critically link phenotypic plasticity to the adaptive potential of biological populations.

View Article: PubMed Central - PubMed

Affiliation: Groningen Institute for Evolutionary Life Sciences, University of Groningen, P.O. Box 11103, Groningen 9700 CC, The Netherlands.

ABSTRACT
Organisms have a remarkable capacity to respond to environmental change. They can either respond directly, by means of phenotypic plasticity, or they can slowly adapt through evolution. Yet, how phenotypic plasticity links to evolutionary adaptability is largely unknown. Current studies of plasticity tend to adopt a phenomenological reaction norm (RN) approach, which neglects the mechanisms underlying plasticity. Focusing on a concrete question - the optimal timing of bacterial sporulation - we here also consider a mechanistic approach, the evolution of a gene regulatory network (GRN) underlying plasticity. Using individual-based simulations, we compare the RN and GRN approach and find a number of striking differences. Most importantly, the GRN model results in a much higher diversity of responsive strategies than the RN model. We show that each of the evolved strategies is pre-adapted to a unique set of unseen environmental conditions. The regulatory mechanisms that control plasticity therefore critically link phenotypic plasticity to the adaptive potential of biological populations.

No MeSH data available.


Related in: MedlinePlus