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Fluctuating natural selection accounts for the evolution of diversification bet hedging.

ABSTRACT: Natural environments are characterized by unpredictability over all time scales. This stochasticity is expected on theoretical grounds to result in the evolution of 'bet-hedging' traits that maximize the long term, or geometric mean fitness even though such traits do not maximize fitness over shorter time scales. The geometric mean principle is thus central to our interpretation of optimality and adaptation; however, quantitative empirical support for bet hedging is lacking. Here, I report a quantitative test using the timing of seed germination-a model diversification bet-hedging trait-in Lobelia inflata under field conditions. In a phenotypic manipulation study, I find the magnitude of fluctuating selection acting on seed germination timing-across 70 intervals throughout five seasons-to be extreme: fitness functions for survival are complex and multimodal within seasons and significantly dissimilar among seasons. I confirm that the observed magnitude of fluctuating selection is sufficient to account for the degree of diversification behaviour characteristic of individuals of this species. The geometric mean principle has been known to economic theory for over two centuries; this study now provides a quantitative test of optimality of a bet-hedging trait in nature.

SUBMITTER: Simons AM

PROVIDER: S-EPMC2677257 | biostudies-literature | 2009 Jun

REPOSITORIES: biostudies-literature

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Fluctuating natural selection accounts for the evolution of diversification bet hedging.

Simons Andrew M AM

Proceedings. Biological sciences 20090304 1664

Natural environments are characterized by unpredictability over all time scales. This stochasticity is expected on theoretical grounds to result in the evolution of 'bet-hedging' traits that maximize the long term, or geometric mean fitness even though such traits do not maximize fitness over shorter time scales. The geometric mean principle is thus central to our interpretation of optimality and adaptation; however, quantitative empirical support for bet hedging is lacking. Here, I report a qua ...[more]

PMID: 19324774

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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

Fluctuating natural selection accounts for the evolution of diversification bet hedging.

Publications

Fluctuating natural selection accounts for the evolution of diversification bet hedging.

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