Experimental evolution of bet hedging in rotifer diapause traits as a response to environmental unpredictability

Abstract Environmental unpredictability results in the evolution of bet-hedging traits, which maximize long-term fitness but are, by definition, suboptimal over short time scales. However, because suboptimal traits are expected to be purged by selection in the shorter term, the persistence of bet hedging remains perplexing. Here, we test the hypothesis that bet hedging persists through the evolution of constraint on short-term adaptation. We experimentally evolve Saccharomyces cerevisiae across two sequential treatments in which the frequency of extreme heat shocks decreases. We predict that experimental evolution under lower frequency heat shocks will result in greater adaptive constraint, or “purge-resistant” bet hedging. Constraint is assayed as evolutionary persistence of heat shock tolerance (HST) under constant benign conditions. As predicted, we find the retention of HST only in lines evolved under reduced frequency detrimental conditions. Results help explain the evolution of bet hedging, and challenge the traditional view that evolutionary constraint is inherently maladaptive.

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Faculty Opinions recommendation of Experimental evolution of bet hedging.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1167007.707056 ◽

2009 ◽

Author(s):

James Moir

Keyword(s):

Experimental Evolution ◽

Bet Hedging

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A continuum of biological adaptations to environmental fluctuation

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2019.1623 ◽

2019 ◽

Vol 286 (1912) ◽

pp. 20191623 ◽

Cited By ~ 1

Author(s):

Ming Liu ◽

Dustin R. Rubenstein ◽

Wei-Chung Liu ◽

Sheng-Feng Shen

Keyword(s):

Overlapping Generations ◽

Bet Hedging ◽

Environmental Fluctuation ◽

Infinite Population ◽

Biological Adaptation ◽

Hedging Strategies ◽

Wide Range ◽

Population Sizes ◽

Environmental Unpredictability ◽

Per Capita

Bet-hedging—a strategy that reduces fitness variance at the expense of lower mean fitness among different generations—is thought to evolve as a biological adaptation to environmental unpredictability. Despite widespread use of the bet-hedging concept, most theoretical treatments have largely made unrealistic demographic assumptions, such as non-overlapping generations and fixed or infinite population sizes. Here, we extend the concept to consider overlapping generations by defining bet-hedging as a strategy with lower variance and mean per capita growth rate across different environments. We also define an opposing strategy—the rising-tide—that has higher mean but also higher variance in per capita growth. These alternative strategies lie along a continuum of biological adaptions to environmental fluctuation. Using stochastic Lotka–Volterra models to explore the evolution of the rising-tide versus bet-hedging strategies, we show that both the mean environmental conditions and the temporal scales of their fluctuations, as well as whether population dynamics are discrete or continuous, are crucial in shaping the type of strategy that evolves in fluctuating environments. Our model demonstrates that there are likely to be a wide range of ways that organisms with overlapping generations respond to environmental unpredictability beyond the classic bet-hedging concept.

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Biological adaptation under fluctuating selection

10.1101/457762 ◽

2018 ◽

Author(s):

Ming Liu ◽

Dustin R. Rubenstein ◽

Wei-Chung Liu ◽

Sheng-Feng Shen

Keyword(s):

Evolutionary Strategy ◽

Bet Hedging ◽

Negative Effects ◽

Fluctuating Selection ◽

Hedging Strategy ◽

Biological Adaptation ◽

Wide Range ◽

Population Sizes ◽

Mean And Variance ◽

Environmental Unpredictability

AbstractBet-hedging—an evolutionary strategy that reduces fitness variance at the expense of lower mean fitness—is the primary explanation for most forms of biological adaptation to environmental unpredictability. However, most applications of bet-hedging theory to biological problems have largely made unrealistic demographic assumptions, such as non-overlapping generations and fixed population sizes. Consequently, the generality and applicability of bet-hedging theory to real world phenomena remains unclear. Here we use continuous-time, stochastic Lotka-Volterra models to relax overly restrictive demographic assumptions and explore a suite of biological adaptations to fluctuating environments. We discover a novel “rising-tide strategy” that—unlike the bet-hedging strategy—generates both a higher mean and variance in fitness. The positive fitness effects of the rising-tide strategy’s specialization to good years can overcome any negative effects of higher fitness variance in unpredictable environments. Moreover, we show not only that the rising-tide strategy will be selected for over a much broader range of environmental conditions than the bet-hedging strategy, but also under more realistic demographic circumstances. Ultimately, our model demonstrates that there are likely to be a wide range of ways that organisms respond to environmental unpredictability.

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Using experimental evolution to understand the persistence of bet-hedging traits in Saccharomyces cerevisiae

10.22215/etd/2020-13890 ◽

2020 ◽

Author(s):

Shravan Raghu

Keyword(s):

Saccharomyces Cerevisiae ◽

Experimental Evolution ◽

Bet Hedging

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Adaptation to temporally fluctuating environments by the evolution of maternal effects

10.1101/023044 ◽

2015 ◽

Cited By ~ 1

Author(s):

Snigdhadip Dey ◽

Steve Proulx ◽

Henrique Teotonio

Keyword(s):

Maternal Effects ◽

Experimental Evolution ◽

Reproductive Strategies ◽

Correlated Response ◽

Bet Hedging ◽

Offspring Performance ◽

Trade Offs ◽

Wide Range ◽

Fluctuating Environments ◽

Selection For

Most organisms live in ever-challenging temporally fluctuating environments. Theory suggests that the evolution of anticipatory (or deterministic) maternal effects underlies adaptation to environments that regularly fluctuate every other generation because of selection for increased offspring performance. Evolution of maternal bet-hedging reproductive strategies that randomize offspring phenotypes is in turn expected to underlie adaptation to irregularly fluctuating environments. Although maternal effects are ubiquitous their adaptive significance is unknown since they can easily evolve as a correlated response to selection for increased maternal performance. Using the nematode Caenorhabditis elegans, we show the experimental evolution of maternal provisioning of offspring with glycogen, in populations facing a novel anoxia hatching environment every other generation. As expected with the evolution of deterministic maternal effects, improved embryo hatching survival under anoxia evolved at the expense of fecundity and glycogen provisioning when mothers experienced anoxia early in life. Unexpectedly, populations facing an irregularly fluctuating anoxia hatching environment failed to evolve maternal bet-hedging reproductive strategies. Instead, adaptation in these populations should have occurred through the evolution of balancing trade-offs over multiple generations, since they evolved reduced fitness over successive generations in anoxia but did not go extinct during experimental evolution. Mathematical modelling confirms our conclusion that adaptation to a wide range of patterns of environmental fluctuations hinges on the existence of deterministic maternal effects, and that they are generally much more likely to contribute to adaptation than maternal bet-hedging reproductive strategies.

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