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Short-term insurance versus long-term bet-hedging strategies as adaptations to variable environments.

ABSTRACT: Understanding how organisms adapt to environmental variation is a key challenge of biology. Central to this are bet-hedging strategies that maximize geometric mean fitness across generations, either by being conservative or diversifying phenotypes. Theoretical models have identified environmental variation across generations with multiplicative fitness effects as driving the evolution of bet-hedging. However, behavioral ecology has revealed adaptive responses to additive fitness effects of environmental variation within lifetimes, either through insurance or risk-sensitive strategies. Here, we explore whether the effects of adaptive insurance interact with the evolution of bet-hedging by varying the position and skew of both arithmetic and geometric mean fitness functions. We find that insurance causes the optimal phenotype to shift from the peak to down the less steeply decreasing side of the fitness function, and that conservative bet-hedging produces an additional shift on top of this, which decreases as adaptive phenotypic variation from diversifying bet-hedging increases. When diversifying bet-hedging is not an option, environmental canalization to reduce phenotypic variation is almost always favored, except where the tails of the fitness function are steeply convex and produce a novel risk-sensitive increase in phenotypic variance akin to diversifying bet-hedging. Importantly, using skewed fitness functions, we provide the first model that explicitly addresses how conservative and diversifying bet-hedging strategies might coexist.

SUBMITTER: Haaland TR

PROVIDER: S-EPMC6590291 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Short-term insurance versus long-term bet-hedging strategies as adaptations to variable environments.

Haaland Thomas Ray TR Wright Jonathan J Tufto Jarle J Ratikainen Irja Ida II

Evolution; international journal of organic evolution 20181226 2

Understanding how organisms adapt to environmental variation is a key challenge of biology. Central to this are bet-hedging strategies that maximize geometric mean fitness across generations, either by being conservative or diversifying phenotypes. Theoretical models have identified environmental variation across generations with multiplicative fitness effects as driving the evolution of bet-hedging. However, behavioral ecology has revealed adaptive responses to additive fitness effects of envir ...[more]

PMID: 30549260

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Project description:Bacterial cells, like many other organisms, face a tradeoff between longevity and fecundity. Planktonic cells are fast growing and fragile, while biofilm cells are often slower growing but stress resistant. Here we ask why bacterial lineages invest simultaneously in both fast- and slow-growing types. We develop a population dynamic model of lineage expansion across a patchy environment and find that mixed investment is favored across a broad range of environmental conditions, even when transmission is entirely via biofilm cells. This mixed strategy is favored because of a division of labor where exponentially dividing planktonic cells can act as an engine for the production of future biofilm cells, which grow more slowly. We use experimental evolution to test our predictions and show that phenotypic heterogeneity is persistent even under selection for purely planktonic or purely biofilm transmission. Furthermore, simulations suggest that maintenance of a biofilm subpopulation serves as a cost-effective hedge against environmental uncertainty, which is also consistent with our experimental findings.IMPORTANCE Cell types specialized for survival have been observed and described within clonal bacterial populations for decades, but why are these specialists continually produced under benign conditions when such investment comes at a high reproductive cost? Conversely, when survival becomes an imperative, does it ever benefit the population to maintain a pool of rapidly growing but vulnerable planktonic cells? Using a combination of mathematical modeling, simulations, and experiments, we find that mixed investment strategies are favored over a broad range of environmental conditions and rely on a division of labor between cell types, where reproductive specialists amplify survival specialists, which can be transmitted through the environment with a limited mortality rate. We also show that survival specialists benefit rapidly growing populations by serving as a hedge against unpredictable changes in the environment. These results help to clarify the general evolutionary and ecological forces that can generate and maintain diverse subtypes within clonal bacterial populations.

Dataset Information

Short-term insurance versus long-term bet-hedging strategies as adaptations to variable environments.

Publications

Short-term insurance versus long-term bet-hedging strategies as adaptations to variable environments.

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