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Experimental evolution of bet hedging under manipulated environmental uncertainty in Neurospora crassa.

ABSTRACT: All organisms are faced with environmental uncertainty. Bet-hedging theory expects unpredictable selection to result in the evolution of traits that maximize the geometric-mean fitness even though such traits appear to be detrimental over the shorter term. Despite the centrality of fitness measures to evolutionary analysis, no direct test of the geometric-mean fitness principle exists. Here, we directly distinguish between predictions of competing fitness maximization principles by testing Cohen's 1966 classic bet-hedging model using the fungus Neurospora crassa. The simple prediction is that propagule dormancy will evolve in proportion to the frequency of 'bad' years, whereas the prediction of the alternative arithmetic-mean principle is the evolution of zero dormancy as long as the expectation of a bad year is less than 0.5. Ascospore dormancy fraction in N. crassa was allowed to evolve under five experimental selection regimes that differed in the frequency of unpredictable 'bad years'. Results were consistent with bet-hedging theory: final dormancy fraction in 12 genetic lineages across 88 independently evolving samples was proportional to the frequency of bad years, and evolved both upwards and downwards as predicted from a range of starting dormancy fractions. These findings suggest that selection results in adaptation to variable rather than to expected environments.

SUBMITTER: Graham JK

PROVIDER: S-EPMC4071552 | biostudies-literature | 2014 Jul

REPOSITORIES: biostudies-literature

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Experimental evolution of bet hedging under manipulated environmental uncertainty in Neurospora crassa.

Graham Jeffrey K JK Smith Myron L ML Simons Andrew M AM

Proceedings. Biological sciences 20140701 1787

All organisms are faced with environmental uncertainty. Bet-hedging theory expects unpredictable selection to result in the evolution of traits that maximize the geometric-mean fitness even though such traits appear to be detrimental over the shorter term. Despite the centrality of fitness measures to evolutionary analysis, no direct test of the geometric-mean fitness principle exists. Here, we directly distinguish between predictions of competing fitness maximization principles by testing Cohen ...[more]

PMID: 24870047

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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

Experimental evolution of bet hedging under manipulated environmental uncertainty in Neurospora crassa.

Publications

Experimental evolution of bet hedging under manipulated environmental uncertainty in Neurospora crassa.

Similar Datasets

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