Abstract
Organisms use various strategies to cope with fluctuating environmental conditions. In diversified bet‐hedging, a single genotype exhibits phenotypic heterogeneity with the expectation that some individuals will survive transient selective pressures. To date, empirical evidence for bet‐hedging is scarce. Here, we observe that individual Drosophila melanogaster flies exhibit striking variation in light‐ and temperature‐preference behaviors. With a modeling approach that combines real world weather and climate data to simulate temperature preference‐dependent survival and reproduction, we find that a bet‐hedging strategy may underlie the observed interindividual behavioral diversity. Specifically, bet‐hedging outcompetes strategies in which individual thermal preferences are heritable. Animals employing bet‐hedging refrain from adapting to the coolness of spring with increased warm‐seeking that inevitably becomes counterproductive in the hot summer. This strategy is particularly valuable when mean seasonal temperatures are typical, or when there is considerable fluctuation in temperature within the season. The model predicts, and we experimentally verify, that the behaviors of individual flies are not heritable. Finally, we model the effects of historical weather data, climate change, and geographic seasonal variation on the optimal strategies underlying behavioral variation between individuals, characterizing the regimes in which bet‐hedging is advantageous.
Highlights
The temperature experience of fly i on day j was determined as pi × shadeDiff × cloudCoverj + Tj, where pi is the thermal preference index of fly i, shadeDiff is the temperature difference between light and shade, cloudCoverj is the average fraction of cloud cover on day j, and Tj is the in-shade temperature on day j
The birth and death rate parameters were identified as the unique pair of values that satisfy two assumptions: (1) the fly population neither grows nor diminishes across the breeding season, that is, it is at numerical equilibrium, and 2) the mean thermal preference index does not evolve across the breeding season, that is, flies are adapted to typical conditions
A MODEL TO COMPARE ADAPTIVE TRACKING AND BET-HEDGING STRATEGIES Could the observed behavioral individuality represent a bethedging strategy to increase the probability that at least some individuals will be well adapted to the current weather conditions? To test this, we proposed a model of fly development and reproduction (Figs. 2A and S2.) in which an individual animal’s behavior could be treated either as perfectly inherited from the mother, or as nonheritable/stochastic variation indicative of a bet-hedging strategy (BH)
Summary
Animals employing bet-hedging refrain from adapting to the coolness of spring with increased warm-seeking that inevitably becomes counterproductive in the hot summer This strategy is valuable when mean seasonal temperatures are typical, or when there is considerable fluctuation in temperature within the season. There are limitations to plasticity (DeWitt et al 1998; Murren et al 2015), such as the metabolic cost of encoding a lookup table, and the speed with which an organism can change its phenotype The latter constraint, phenotypic inflexibility, applies to animals, such as insects, that attain a final adult life stage. Populations can survive changing conditions by having diversified phenotypes as a result of genetic variation; this allows organisms to readily evolve/adapt to new conditions. Evolution published by Wiley Periodicals, Inc. on behalf of The Society for the Study of Evolution
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