Conservative Bet-hedging Research Articles

Bet-hedging via dispersal aids the evolution of plastic responses to unreliable cues.

Adaptive plasticity is expected to evolve when informative cues predict environmental variation. However, plastic responses can be maladaptive even when those cues are informative, if prediction mistakes are shared across members of a generation. These fitness costs can constrain the evolution of plasticity when initial plastic mutants use of cues of only moderate reliability. Here, we model the barriers to the evolution of plasticity produced by these constraints and show that dispersal across a metapopulation can overcome them. Constraints are also lessened, though not eliminated, when plastic responses are free to evolve gradually and in concert with increased reliability. Each of these factors be viewed as a form of bet-hedging: by lessening correlations in the fates of relatives, dispersal acts as diversifying bet-hedging, while producing submaximal responses to a cue can be understood as a conservative bet-hedging strategy. While poor information may constrain the evolution of plasticity, the opportunity for bet-hedging may predict when that constraint can be overcome.

The evolution of social learning as phenotypic cue integration.

Most analyses of the origins of cultural evolution focus on when and where social learning prevails over individual learning, overlooking the fact that there are other developmental inputs that influence phenotypic fit to the selective environment. This raises the question of how the presence of other cue 'channels' affects the scope for social learning. Here, we present a model that considers the simultaneous evolution of (i) multiple forms of social learning (involving vertical or horizontal learning based on either prestige or conformity biases) within the broader context of other evolving inputs on phenotype determination, including (ii) heritable epigenetic factors, (iii) individual learning, (iv) environmental and cascading maternal effects, (v) conservative bet-hedging, and (vi) genetic cues. In fluctuating environments that are autocorrelated (and hence predictable), we find that social learning from members of the same generation (horizontal social learning) explains the large majority of phenotypic variation, whereas other cues are much less important. Moreover, social learning based on prestige biases typically prevails in positively autocorrelated environments, whereas conformity biases prevail in negatively autocorrelated environments. Only when environments are unpredictable or horizontal social learning is characterized by an intrinsically low information content, other cues such as conservative bet-hedging or vertical prestige biases prevail. This article is part of the theme issue 'Foundations of cultural evolution'.

Transgenerational Plasticity and Bet-Hedging: A Framework for Reaction Norm Evolution

Decision-making under uncertain conditions favors bet-hedging (avoidance of fitness variance), whereas predictable environments favor phenotypic plasticity. However, entirely predictable or entirely unpredictable conditions are rarely found in nature. Intermediate strategies are required when the time lag between information sensing and phenotype induction is large (e.g., transgenerational plasticity) and when cues are only partially predictive of future conditions. Nevertheless, current theory regards plasticity and bet-hedging as distinct entities. We here develop a unifying framework: based on traits with binary outcomes like seed germination or diapause incidence we clarify that diversified bet-hedging (risk-spreading among one’s offspring) and transgenerational plasticity are mutually exclusive strategies, arising from opposing changes in reaction norms (allocating phenotypic variance among or within environments). We further explain the relationship of this continuum with arithmetic mean maximization vs. conservative bet-hedging (a risk-avoidance strategy), and canalization vs. phenotypic variance in a three-dimensional continuum of reaction norm evolution. We discuss under which scenarios costs and limits may constrain the evolution of reaction norm shapes.

Bet-hedging across generations can affect the evolution of variance-sensitive strategies within generations.

In order to understand how organisms cope with ongoing changes in environmental variability, it is necessary to consider multiple adaptations to environmental uncertainty on different time scales. Conservative bet-hedging (CBH) represents a long-term genotype-level strategy maximizing lineage geometric mean fitness in stochastic environments by decreasing individual fitness variance, despite also lowering arithmetic mean fitness. Meanwhile, variance-prone (aka risk-prone) strategies produce greater variance in short-term payoffs, because this increases expected arithmetic mean fitness if the relationship between payoffs and fitness is accelerating. Using evolutionary simulation models, we investigate whether selection for such variance-prone strategies is counteracted by selection for bet-hedging that works to adaptively reduce fitness variance. In our model, variance proneness evolves in fine-grained environments (lower correlations among individuals in energetic state and/or payoffs), and with larger numbers of independent decision events over which resources accumulate prior to selection. Conversely, multiplicative fitness accumulation, caused by coarser environmental grain and fewer decision events selection, favours CBH via greater variance aversion. We discuss examples of variance-sensitive strategies in optimal foraging, migration, life histories and cooperative breeding using this bet-hedging perspective. By linking disparate fields of research studying adaptations to variable environments, we should be better able to understand effects of human-induced rapid environmental change.

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

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.

The evolution of different maternal investment strategies in two closely related desert vertebrates.

We compared egg size phenotypes and tested several predictions from the optimal egg size (OES) and bet‐hedging theories in two North American desert‐dwelling sister tortoise taxa, Gopherus agassizii and G. morafkai, that inhabit different climate spaces: relatively unpredictable and more predictable climate spaces, respectively. Observed patterns in both species differed from the predictions of OES in several ways. Mean egg size increased with maternal body size in both species. Mean egg size was inversely related to clutch order in G. agassizii, a strategy more consistent with the within‐generation hypothesis arising out of bet‐hedging theory or a constraint in egg investment due to resource availability, and contrary to theories of density dependence, which posit that increasing hatchling competition from later season clutches should drive selection for larger eggs. We provide empirical evidence that one species, G. agassizii, employs a bet‐hedging strategy that is a combination of two different bet‐hedging hypotheses. Additionally, we found some evidence for G. morafkai employing a conservative bet‐hedging strategy. (e.g., lack of intra‐ and interclutch variation in egg size relative to body size). Our novel adaptive hypothesis suggests the possibility that natural selection favors smaller offspring in late‐season clutches because they experience a more benign environment or less energetically challenging environmental conditions (i.e., winter) than early clutch progeny, that emerge under harsher and more energetically challenging environmental conditions (i.e., summer). We also discuss alternative hypotheses of sexually antagonistic selection, which arise from the trade‐offs of son versus daughter production that might have different optima depending on clutch order and variation in temperature‐dependent sex determination (TSD) among clutches. Resolution of these hypotheses will require long‐term data on fitness of sons versus daughters as a function of incubation environment, data as yet unavailable for any species with TSD.

The evolution of optimal emergence times: bet hedging and the quest for an ideal free temporal distribution of individuals

Proper timing of activities is one of the principal challenges faced by most organisms. Organisms need to account for various aspects in decision making like avoiding inordinate risks, synchronizing with resource availability, or finding mates. We provide analytical and simulation models to investigate the influence of life expectancy, resource competition and unpredictable environmental conditions (environmental uncertainty) on the evolutionarily stable distribution of emergence times in organisms depending on seasonally available resources. We focus on the partitioning of total phenotypic variance in emergence times into 1) genetic variance in mean emergence times between lineages and 2) environmental trait variance that determines the intra‐lineage variance in the timing of emergence.Both, life expectancy of organisms and intensity of competition severely influence the evolutionary response to environmental uncertainty. Our main findings can be summarized as follows: 1) in general diversifying bet hedging (environmental trait variance) is the adequate mechanism to reduce the risk arising from environmental uncertainty while conservative bet hedging, i.e. delaying emergence into ‘safe’ phases of the season is restricted to short lived organisms and to situations with vanishing competition. 2) Environmental trait variance increases with increasing environmental uncertainty whereas 3) significant genetic variance evolves only under severe resource competition; it is driven by selection for an ideal free distribution of emergence times. 4) The level of genetic variance evolving declines with increasing life expectancy of organisms. 5) With sufficiently short life expectancy evolutionary branching and coexistence of distinctly different emergence strategies occurs; the number of co‐occurring strategies is determined by the level of environmental uncertainty.Our model provides cues for understanding how different ecological factors contribute and interact to shape the evolution of emergence strategies.

Adaptation to Temporally Fluctuating Environments by the Evolution of Maternal Effects.

All organisms live in temporally fluctuating environments. Theory predicts that the evolution of deterministic maternal effects (i.e., anticipatory maternal effects or transgenerational phenotypic plasticity) underlies adaptation to environments that fluctuate in a predictably alternating fashion over maternal-offspring generations. In contrast, randomizing maternal effects (i.e., diversifying and conservative bet-hedging), are expected to evolve in response to unpredictably fluctuating environments. Although maternal effects are common, evidence for their adaptive significance is equivocal since they can easily evolve as a correlated response to maternal selection and may or may not increase the future fitness of offspring. Using the hermaphroditic nematode Caenorhabditis elegans, we here show that the experimental evolution of maternal glycogen provisioning underlies adaptation to a fluctuating normoxia–anoxia hatching environment by increasing embryo survival under anoxia. In strictly alternating environments, we found that hermaphrodites evolved the ability to increase embryo glycogen provisioning when they experienced normoxia and to decrease embryo glycogen provisioning when they experienced anoxia. At odds with existing theory, however, populations facing irregularly fluctuating normoxia–anoxia hatching environments failed to evolve randomizing maternal effects. Instead, adaptation in these populations may have occurred through the evolution of fitness effects that percolate over multiple generations, as they maintained considerably high expected growth rates during experimental evolution despite evolving reduced fecundity and reduced embryo survival under one or two generations of anoxia. We develop theoretical models that explain why adaptation to a wide range of patterns of environmental fluctuations hinges on the existence of deterministic maternal effects, and that such deterministic maternal effects are more likely to contribute to adaptation than randomizing maternal effects.

Flexible dispersal dimorphism in zooplankton resting eggs: an example of repeated phenotypic coin flipping?

Theory predicts that spatio-temporal variation in habitat suitability will promote selection for dispersal. In addition to movement in space, dispersal gains an extra dimension in freshwater zooplankton because resting eggs can disperse in time as well, via dormancy. Potential trade-offs between both strategies, however, remain largely unexplored. Using a temporary pool fairy shrimp population as a model, we tested for consistent differences in buoyancy among resting eggs during consecutive inundations in a standardized laboratory experiment and explored a potential trade-off between dispersal (floaters versus sinkers) and dormancy (high versus low hatching fractions). Although discrete dispersal morphs were present, this trait was not fixed. Irrespective of their dispersal phenotype during previous inundations, floating eggs hatched more frequently than sinking eggs. Egg morphology did not affect buoyancy and, between inundations, approximately half of the eggs changed their dispersal phenotype. Although this mechanism has affinities with conservative bet hedging and adaptive coin flipping, it is unique because the dispersal phenotype can switch at the onset of each inundation. Despite possible selection against dispersal at the population level, such a strategy ensures variation in dispersal ability at any moment and could promote population persistence in a metapopulation context. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 749–756.

Phenotypic stochasticity protects lytic bacteriophage populations from extinction during the bacterial stationary phase.

It is generally thought that the adsorption rate of a bacteriophage correlates positively with fitness, but this view neglects that most phages rely only on exponentially growing bacteria for productive infections. Thus, phages must cope with the environmental stochasticity that is their hosts’ physiological state. If lysogeny is one alternative, it is unclear how strictly lytic phages can survive the host stationary phase. Three scenarios may explain their maintenance: (1) pseudolysogeny, (2) diversified, or (3) conservative bet hedging. To better understand how a strictly lytic phage survives the stationary phase of its host, and how phage adsorption rate impacts this survival, we challenged two strictly lytic phage λ, differing in their adsorption rates, with stationary phase Escherichia coli cells. Our results showed that, pseudolysogeny was not responsible for phage survival and that, contrary to our expectation, high adsorption rate was not more detrimental during stationary phase than low adsorption rate. Interestingly, this last observation was due to the presence of the “residual fraction” (phages exhibiting extremely low adsorption rates), protecting phage populations from extinction. Whether this cryptic phenotypic variation is an adaptation (diversified bet hedging) or merely reflecting unavoidable defects during protein synthesis remains an open question.

Nontraditional Life-History Choices: What Can "Intermediates" Tell Us about Evolutionary Transitions between Modes of Invertebrate Development?

Mode of development in marine invertebrates has been largely viewed as a dichotomy between small eggs that develop into free-living planktotrophic larvae and large eggs that bypass the larval stage and develop directly into juveniles. Modes of development that could be categorized as "intermediate" between these two extremes include facultative feeding larvae, short-lived planktotrophic larvae, dispersal dimorphisms, and poecilogony (in which nutritional mode varies within a species). These intermediates are rare. The few species-level phylogenies available that include them do not generally support the interpretation of intermediates as necessary, ephemeral transitional forms. Instead, they support the idea that intermediates are well adapted to their environments but that either these environments are short-lived relative to the frequency of speciation, or speciation events are associated with shifts in the mode of development. Each of the different intermediate forms could have evolved in response to variable environments. The phenotypically plastic intermediates could be a response to predictable environmental variation. Facultative feeding larvae and short-lived planktotrophic larvae could reflect conservative bet-hedging in response to unpredictable environmental variation, whereas poecilogony with mixed clutches could represent the alternative: diversifying bet-hedging. Since environmental variability is common, it remains an enigma why these intermediates are so rare. Discovery of more intermediates, and their careful description in terms of the level of variation expressed within, and among, clutches, and among females and populations, as well as determination of the genetic and environmental influences on this variation, will provide valuable test-cases for theories of the evolution of alternative phenotypes.

Spatial variation in egg size and egg number reflects trade‐offs and bet‐hedging in a freshwater fish

1. Maternal reproductive investment is thought to reflect a trade-off between offspring size and fecundity, and models generally predict that mothers inhabiting adverse environments will produce fewer, larger offspring. More recently, the importance of environmental unpredictability in influencing maternal investment has been considered, with some models predicting that mothers should adopt a diversified bet-hedging strategy whilst others a conservative bet-hedging strategy. 2. We explore spatial egg size and fecundity patterns in the freshwater fish southern pygmy perch (Nannoperca australis) that inhabits a diversity of streams along gradients of environmental quality, variability and predictability. 3. Contrary to some predictions, N.australis populations inhabiting increasingly harsh streams produced more numerous and smaller eggs. Furthermore, within-female egg size variability increased as environments became more unpredictable. 4. We argue that in harsh environments or those prone to physical disturbance, sources of mortality are size independent with offspring size having only a minor influence on offspring fitness. Instead, maternal fitness is maximized by producing many small eggs, increasing the likelihood that some offspring will disperse to permanent water. We also provide empirical support for diversified bet-hedging as an adaptive strategy when future environmental quality is uncertain and suggest egg size may be a more appropriate fitness measure in stable environments characterized by size-dependent fitness. These results likely reflect spatial patterns of adaptive plasticity and bet-hedging in response to both predictable and unpredictable environmental variance and highlight the importance of considering both trait averages and variance. 5. Reproductive life-history traits can vary predictably along environmental gradients. Human activity, such as the hydrological modification of natural flow regimes, alters the form and magnitude of these gradients, and this can have both ecological and evolutionary implications for biota adapted to now non-existent natural environmental heterogeneity.

Fecundity, Offspring Longevity, and Assortative Mating: Parametric Tradeoffs in Sexual and Life History Strategy

Genetic diversification of offspring represents a bet-hedging strategy that evolved as an adaptation to unpredictable environments. The benefits of sexual reproduction come with severe costs. For example, each offspring only carries half of each parent's genetic makeup through direct descent. The lower the reproductive rate, the more substantial the cost when considering the proportion of genes represented in subsequent generations. Positive assortative mating represents a conservative bet-hedging strategy that offsets some of these costs and preserves coadapted genomes in stable and predictable environments, whereas negative assortative mating serves the inverse function of genetic diversification in unstable and unpredictable environments.

Bet-hedging as an evolutionary game: the trade-off between egg size and number

Bet-hedging theory addresses how individuals should optimize fitness in varying and unpredictable environments by sacrificing mean fitness to decrease variation in fitness. So far, three main bet-hedging strategies have been described: conservative bet-hedging (play it safe), diversified bet-hedging (don't put all eggs in one basket) and adaptive coin flipping (choose a strategy at random from a fixed distribution). Within this context, we analyse the trade-off between many small eggs (or seeds) and few large, given an unpredictable environment. Our model is an extension of previous models and allows for any combination of the bet-hedging strategies mentioned above. In our individual-based model (accounting for both ecological and evolutionary forces), the optimal bet-hedging strategy is a combination of conservative and diversified bet-hedging and adaptive coin flipping, which means a variation in egg size both within clutches and between years. Hence, we show how phenotypic variation within a population, often assumed to be due to non-adaptive variation, instead can be the result of females having this mixed strategy. Our results provide a new perspective on bet-hedging and stress the importance of extreme events in life history evolution.