High Altitude Frogs (Rana kukonoris) Adopt a Diversified Bethedging Strategy in the Face of Environmental Unpredictability

Environmental unpredictability can influence strategies of maternal investment among eggs within a clutch. Models predict that breeding females should adopt a diversified bet-hedging strategy in unpredictable environments, but empirical field evidence from Asia is scarce. Here we tested this hypothesis by exploring spatial patterns in egg size along an altitudinal gradient in a frog species(Rana kukunoris) inhabiting the Tibetan Plateau. Within-clutch variability in egg size increased as the environment became variable(e.g., lower mean monthly temperature and mean monthly rainfall at higher altitudes), and populations in environments with more unpredictable rainfall produced eggs that were smaller and more variable in size. We provide support for a diversified bet-hedging strategy in high-altitude environments, which experience dynamic weather patterns and therefore are of unpredictable environmental quality. This strategy may be an adaptive response to lower environmental quality and higher unpredictable environmental variance. Such a strategy should increase the likelihood of breeding success and maximize maternal lifetime fitness by producing offspring that are adapted to current environmental conditions. We speculate that in high-altitude environments prone to physical disturbance, breeding females are unable to consistently produce the optimal egg size due to physiological constraints imposed by environmental conditions(e.g., duration of the active season, food availability). Species and populations whose breeding strategies are adapted to cope with uncertain environmental conditions by adjusting offspring size and therefore quality show a remarkable degree of ability to cope with future climatic changes.     

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.     

Generalists versus specialists in fluctuating environments: a bet-hedging perspective

Bet-hedging evolves in fluctuating environments because long-term genotype success is determined by geometric (rather than arithmetic) mean fitness across generations. Diversifying bet-hedging produces different specialist offspring, whereas conservative bet-hedging produces similar generalist offspring. However, many fields, such as behavioral ecology and thermal physiology, typically consider specialist versus generalist strategies only in terms of maximizing arithmetic mean fitness benefits to individuals. Here we model how environmental variability affects optimal amounts of phenotypic variation within and among individuals to maximise genotype fitness, and we disentangle the effects of individual-level optimization and genotype-level bet-hedging by comparing long-term arithmetic versus geometric mean fitness. For traits with additive fitness effects within lifetimes (e.g. foraging-related traits), genotypes of similar generalists or diversified specialists perform equally well. However, if fitness effects are multiplicative within lifetimes (e.g. sequential survival probabilities), generalist individuals are always favored. In this case, geometric mean fitness optimization requires even more within-individual phenotypic variation than does arithmetic mean fitness, causing individuals to be more generalist than required to simply maximize their own expected fitness. In contrast to previous results in the bet-hedging literature, this generalist conservative bet-hedging effect is always favored over diversifying bet-hedging. These results link the evolution of behavioral and ecological specialization with earlier models of bet-hedging, and we apply our framework to a range of natural phenomena from habitat choice to host specificity in parasites.     

Bet-hedging--a triple trade-off between means, variances and correlations

In unpredictably varying environments, strategies that have a reduced variance in fitness can invade a population consisting of individuals that on average do better. Such strategies 'hedge their evolutionary bets' against the variability of the environment. The idea of bet-hedging arises from the fact that appropriate measure of long-term fitness is sensitive to variance, leading to the potential for strategies with a reduced mean fitness to invade and increase in frequency. Our aim is to review the conceptual foundation of bet-hedging as a mechanism that influences short- and long-term evolutionary processes. We do so by presenting a general model showing how evolutionary changes are affected by variance in fitness and how genotypic variance in fitness can be separated into variance in fitness at the level of the individuals and correlations in fitness among them. By breaking down genotypic fitness variance in this way the traditional divisions between conservative and diversified strategies are more easily intuited, and it is also shown that this division can be considered a false dichotomy, and is better viewed as two extreme points on a continuum. The model also sheds light on the ideas of within- and between-generation bet-hedging, which can also be generalized to be seen as two ends of a different continuum. We use a simple example to illustrate the virtues of our general model, as well as discuss the implications for systems where bet-hedging has been invoked as an explanation.     

Evolutionary bet-hedging in the real world: empirical evidence and challenges revealed by plants

Understanding the adaptations that allow species to live in temporally variable environments is essential for predicting how they may respond to future environmental change. Variation at the intergenerational scale can allow the evolution of bet-hedging strategies: a novel genotype may be favoured over an alternative with higher arithmetic mean fitness if the new genotype experiences a sufficiently large reduction in temporal fitness variation; the successful genotype is said to have traded off its mean and variance in fitness in order to ‘hedge its evolutionary bets’. We review the evidence for bet-hedging in a range of simple plant systems that have proved particularly tractable for studying bet-hedging under natural conditions. We begin by outlining the essential theory, reiterating the important distinction between conservative and diversified bet-hedging strategies. We then examine the theory and empirical evidence for the canonical example of bet-hedging: diversification via dormant seeds in annual plants. We discuss the complications that arise when moving beyond this simple case to consider more complex life-history traits, such as flowering size in semelparous perennial plants. Finally, we outline a framework for accommodating these complications, emphasizing the central role that model-based approaches can play.     

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.     

Ectoparasitic Argulus coregoni (Crustacea: Branchiura) hedge their bets – studies on egg hatching dynamics

Unpredictability in the temporal availability of susceptible hosts is likely to act as a selection pressure affecting the life history strategies of parasites. In highly variable environments the future of the lineage can be secured by spreading the risk, for example, by producing descendants that differ in their timing of emergence. Counter to this, in predictable environments a single "best-adapted" phenotype is expected. We asked whether ectoparasitic Argulus coregoni egg hatching pattern can be explained as a genetically canalized individual trait; an instance of phenotypic plasticity or bet-hedging. We collected egg clutches laid by individual A. coregoni females in early and late reproductive period of the lice population and randomized the clutches within 3 treatments. Intra- and inter-clutch variability in the hatching dynamics of A. coregoni eggs was monitored and the reproductive potential assessed. On average A. coregoni females laid 317 (SD±176.6) eggs. We found that the plasticity in the hatching dynamics among A. coregoni eggs was remarkable. Noticeable peaks in hatching were followed each of the repeated artificial "winter treatments" in 1°C. Repeated 2 weeks cold treatments induced relatively bigger hatching peaks than 2 days cold treatments compared to controls at room temperature. However, in all treatments, egg clutches hatched through an extended period of 7 months on average and the total hatching percentages were similar. We found that intra-clutch variability in hatching among eggs laid by single A. coregoni females was greater than inter-clutch variability. Our data support the predictions of the adaptive bet-hedging strategy in relation to egg-hatching dynamics. Response to cooling and bet-hedging may be adaptive for such species like A. coregoni since by synchronizing the life-cycle with the seasonal environment will assist transmission and parasite fitness.     

Dealing with stochastic environmental variation in space and time: bet hedging by generalist,specialist, and diversified strategies

Building on previous work, we derive an optimization model for a two-state stochastic environment and evaluate the fitnesses of five reproductive strategies across generations. To do this, we characterize spatiotemporal variation and define grain (=patch) size as the scale of fitness autocorrelation. Fitness functions of environmental condition are Gaussian. The strategies include two specialists on each of the environmental conditions; two generalists that each fare equally well under both conditions, but one (a conservative bet hedger) optimizes the shape of the fitness function; and a diversified bet hedger producing an optimal mix of the two specialists within individual broods. When the environment is primarily in one of the two states, the specialist on that state achieves the highest fitness. In the more interesting situation where the two environments are equally prevalent in the long term, with low-moderate environmental variation, a generalist strategy (that copes with both states well) does best. Higher variation favors diversified bet hedgers, or surprisingly, specialists, depending mainly on whether spatial or temporal variation predominates. These strategies reduce variance in fitness and optimize the distribution of offspring among patches differently: specialists by spreading offspring among many independently varying patches, while diversified bet hedgers put all offspring into a few patches or a single patch. We distinguish features consistent with strategies like diversified bet hedgers that spread risk in time from features linked to strategies like specialists that spread risk in space. Finally, we present testable hypotheses arising from this study and suggest directions for future work.     

Bet-Hedging Diapause Strategies in Stochastic Environments

In many insect species, adult emergence spreads over several years because of the existence of prolonged diapause in certain individuals. From stochastic models, we show that diversified bet-hedging strategies (mixed strategies with emergence after 1 or 2 yr) are more fit than simple diapause strategy (emergence after 1 yr) or fixed prolonged diapause strategy (emergence after 2 yr) in isolated chestnut weevil populations. This conclusion applies to a large range of survival rates in prolonged diapause and is insensitive to initial conditions, magnitude of temporal autocorrelation, distribution of demographic parameters, and quoted values of population size limitation. However, the shape of the fitness distribution as a function of prolonged diapause frequency changes greatly in the absence of population size limitation. Whatever the survival rate during prolonged diapause, we find that there is no genotypic advantage to extending diapause for all chestnut weevil larvae to more than 1 yr. Our models predict selection of bet-hedging strategies over a large range of prolonged diapause frequencies. This result is consistent with the existence of several mixed strategies in a population. Emergences after 3 yr are not crucial for selection or for the dynamics of mixed strategies in the chestnut weevil.     

Suboptimal timing of reproduction in Lobelia inflata may be a conservative bet-hedging strategy

Age and size at reproduction are important components of fitness, and are variable both within and among angiosperm species. The fitness consequences of such life-history variation are most readily studied in organisms that reproduce only once in their lifetime. The timing of the onset of reproduction (bolting) in the monocarpic perennial, Lobelia inflata, occurs over a range of dates within a season, and may be postponed to a later year. Empirical relationships among life-history traits, derived from over 950 wild-growing and experimentally manipulated plants in the field, are used to model an optimal changing size threshold (norm of reaction) for bolting over the growing season. Comparisons are made between observed and expected norms of reaction governing bolting. An apparently suboptimal bolting schedule that precludes bolting beyond an early (conservative) date is observed, and is found to be qualitatively consistent with conservative bet hedging under unpredictable season lengths. On this basis we propose the schedule of bolting as a plausible example of a conservative bet-hedging strategy. The results underscore the critical need for long-term studies of fluctuating selection to distinguish suboptimality from bet hedging.     

Mating portfolios: bet-hedging,sexual selection and female multiple mating

Polyandry (female multiple mating) has profound evolutionary and ecological implications. Despite considerable work devoted to understanding why females mate multiply, we currently lack convincing empirical evidence to explain the adaptive value of polyandry. Here, we provide a direct test of the controversial idea that bet-hedging functions as a risk-spreading strategy that yields multi-generational fitness benefits to polyandrous females. Unfortunately, testing this hypothesis is far from trivial, and the empirical comparison of the across-generations fitness payoffs of a polyandrous (bet hedger) versus a monandrous (non-bet hedger) strategy has never been accomplished because of numerous experimental constraints presented by most ‘model’ species. In this study, we take advantage of the extraordinary tractability and versatility of a marine broadcast spawning invertebrate to overcome these challenges. We are able to simulate multi-generational (geometric mean) fitness among individual females assigned simultaneously to a polyandrous and monandrous mating strategy. Our approaches, which separate and account for the effects of sexual selection and pure bet-hedging scenarios, reveal that bet-hedging, in addition to sexual selection, can enhance evolutionary fitness in multiply mated females. In addition to offering a tractable experimental approach for addressing bet-hedging theory, our study provides key insights into the evolutionary ecology of sexual interactions.     

Adaptation in a variable environment: Phenotypic plasticity and bet‐hedging during egg diapause and hatching in an annual killifish

Two ways in which organisms adapt to variable environments are phenotypic plasticity and bet‐hedging. Theory suggests that bet‐hedging is expected to evolve in unpredictable environments for which reliable cues indicative of future conditions (or season length) are lacking. Alternatively, if reliable cues exist indicating future conditions, organisms will be under selection to produce the most appropriate phenotype —that is, adaptive phenotypic plasticity. Here, we experimentally test which of these modes of adaptation are at play in killifish that have evolved an annual life cycle. These fish persist in ephemeral pools that completely dry each season through the production of eggs that can remain in developmental arrest, or diapause, buried in the soil, until the following rainy season. Consistent with diversified bet‐hedging (a risk spreading strategy), we demonstrate that the eggs of the annual killifish Nothobranchius furzeri exhibit variation at multiple levels—whether or not different stages of diapause are entered, for how long diapause is entered, and the timing of hatching—and this variation persists after controlling for both genetic and environmental sources of variation. However, we show that phenotypic plasticity is also present in that the proportion of eggs that enter diapause is influenced by environmental factors (temperature and light level) that vary seasonally. In nature there is typically a large parameter zone where environmental cues are somewhat correlated with seasonality, but not perfectly so, such that it may be advantageous to have a combination of both bet‐hedging and plasticity.     

Patterns and fitness consequences of intraclutch variation in egg provisioning in tropical Australian frogs

Intraclutch variation in offspring size should evolve when offspring encounter unpredictable environmental conditions. This form of bet-hedging should maximise the lifetime reproductive success of individuals that engage it. We documented the numbers of eggs and means and variances of yolk volume in 15 frog species that occur in tropical savanna woodland. We experimentally determined the effects of initial yolk volume on larval growth patterns in four species. Intraclutch variation in yolk volume occurred to some degree in all species surveyed. Some species had very low, others had very high, intraclutch variation in yolk volume, but all species in which some clutches were highly variable also produced clutches with low variability. Species that occur in areas where the offspring environment is likely to be unpredictable had elevated levels of intraclutch variation in egg provisioning. There was no trade-off between egg size and number in any species surveyed. Under benign laboratory conditions, tadpoles from eggs with larger yolk volumes hatched at larger sizes, and these size differences persisted through a substantial proportion of the larval stage. This indicates that intraclutch variation in egg size has major offspring and thus parental fitness consequences, and is therefore a functional selection variable. This study provides evidence in support of models which predict that intraclutch variation in offspring provisioning can evolve in organisms that reproduce in unpredictable habitats.     

Mate choice for major histocompatibility complex genetic divergence as a bet-hedging strategy in the Atlantic salmon (Salmo salar)

Major histocompatibility complex (MHC)-dependent mating preferences have been observed across vertebrate taxa and these preferences are expected to promote offspring disease resistance and ultimately, viability. However, little empirical evidence linking MHC-dependent mate choice and fitness is available, particularly in wild populations. Here, we explore the adaptive potential of previously observed patterns of MHC-dependent mate choice in a wild population of Atlantic salmon (Salmo salar) in Québec, Canada, by examining the relationship between MHC genetic variation and adult reproductive success and offspring survival over 3 years of study. While Atlantic salmon choose their mates in order to increase MHC diversity in offspring, adult reproductive success was in fact maximized between pairs exhibiting an intermediate level of MHC dissimilarity. Moreover, patterns of offspring survival between years 0+ and 1+, and 1+ and 2+ and population genetic structure at the MHC locus relative to microsatellite loci indicate that strong temporal variation in selection is likely to be operating on the MHC. We interpret MHC-dependent mate choice for diversity as a likely bet-hedging strategy that maximizes parental fitness in the face of temporally variable and unpredictable natural selection pressures.     

ADAPTIVE DYNAMICS OF DORMANCY DURATION VARIABILITY: EVOLUTIONARY TRADE-OFF AND PRIORITY EFFECT LEAD TO SUBOPTIMAL ADAPTATION

Many plants, insects, and crustaceans show within-population variability in dormancy length. The question of whether such variability corresponds to a genetic polymorphism of pure strategies or a mixed bet-hedging strategy, and how the level of phenotypic variability can evolve remain unknown for most species. Using an eco-genetic model rooted in a 25-year ecological field study of a Chestnut weevil, Curculio elephas , we show that its diapause-duration variability is more likely to have evolved by the spread of a bet-hedging strategy than by the establishment of a genetic polymorphism. Investigating further the adaptive dynamics of diapause-duration variability, we find two unanticipated patterns of general interest. First, there is a trade-off between the ability of bet-hedging strategies to persist on an ecological time scale and their ability to invade. The optimal strategy (in terms of persistence) cannot invade, whereas suboptimal bet-hedgers are good invaders. Second, we describe an original evolutionary dynamics where each bet-hedging strategy (defined by its rate of prolonged diapause) resists invasion by all others, so that the first type of bet-hedger to appear persists on an evolutionary time scale. Such "evolutionary priority effect" could drive the evolution of maladapted levels of diapause-duration variability.     

Sibling-size variation in brown trout Salmo trutta in relation to egg size and stream size

Sibling-size variation (SSV), estimated as the coefficient of variation of egg size, was investigated for 13 populations of brown trout Salmo trutta . SSV was negatively correlated with mean egg size both at the population and individual levels. After correction for the effect of mean egg size, SSV was also negatively correlated with stream size. These results provide new information about how salmonid SSV can vary at different ecological scales (individual, population and region). The results are discussed in light of competing theories for explaining SSV: (1) the passive effect hypothesis, stating that egg size variation follows passively from selection on egg size and (2) the bet-hedging hypothesis, stating that high SSV is adaptive in unpredictable environments.     

Female multiple mating as a genetic bet-hedging strategy when mate choice criteria are unreliable

Female multiple mating (or polyandry) is considered to act as a genetic bet-hedging mechanism, by which females can reduce the assessment error in regard to mates genetic quality when only uncertain information is available. In spite of frequent verbal arguments, no theoretical examination has been carried out to determine the effectiveness of bet-hedging by multiple mating. In the present paper, I show that three factors, female population size, remating costs and environmental fluctuation, all affect the effectiveness of bet-hedging. A mathematical model predicts that bet-hedging effectively works only in small populations, and computer simulations were used to confirm this prediction. The results of simulations differed according to the degree of environmental fluctuation. In relatively stable environments, if there is no remating cost, the fixation probability of a multiple mating strategy is slightly higher than that of a single mating strategy, independent of female population size. However, with very slight fitness costs, multiple mating drastically loses its advantage as population size increases, and almost always becomes extinct within large populations. This means that the evolution of polyandry solely by the mechanism of bet-hedging is unlikely in stable environments. However, in unpredictable environments, or when negative frequency-dependent selection on fitness-related loci is introduced, a multiple mating strategy is sometimes successful against a single mating strategy, even if it entails a small fitness cost. Therefore, female multiple mating may possibly evolve only in these limited conditions. In most cases, some deterministic mechanisms such as postcopulatory sperm selection by multiply mated females (or direct material benefits) are more reasonable as the evolutionary causes of polyandry.     

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.     

Diapause and bet-hedging strategies in insects: a meta-analysis of reaction norm shapes

Many organisms escape from lethal climatological conditions by entering a resistant resting stage called diapause, which needs to be optimally timed with seasonal change. As climate change exerts selection pressure on phenology, the evolution of mean diapause timing, but also of phenotypic plasticity and bet-hedging strategies is expected. The potential of the latter strategy as a means of coping with environmental unpredictability has received little attention in the climate change literature. Populations should be adapted to spatial variation in local conditions; contemporary patterns of phenological strategies across a geographic range may hence provide information about their evolvability. We thus extracted 458 diapause reaction norms from 60 studies. First, we correlated mean diapause timing with mean winter onset. Then we partitioned the reaction norm variance into a temporal component (phenotypic plasticity) and among-offspring variance (diversified bet-hedging) and correlated this variance composition with variability of winter onset. Mean diapause timing correlated reasonably well with mean winter onset, except for populations at high latitudes, which apparently failed to track early onsets. Variance among offspring was, however, limited and correlated only weakly with environmental variability, indicating little scope for bet-hedging. The apparent lack of phenological bet-hedging strategies may pose a risk in a less predictable climate, but we also highlight the need for more data on alternative strategies.     

Climate mediates the success of migration strategies in a marine predator

Individual behavioural specialisation has far‐reaching effects on fitness and population persistence. Theory predicts that unconditional site fidelity, that is fidelity to a site independent of past outcome, provides a fitness advantage in unpredictable environments. However, the benefits of alternative site fidelity strategies driving intraspecific variation remain poorly understood and have not been evaluated in different environmental contexts. We show that contrary to expectation, strong and weak site fidelity strategies in migratory northern elephant seals performed similarly over 10 years, but the success of each strategy varied interannually and was strongly mediated by climate conditions. Strong fidelity facilitated stable energetic rewards and low risk, while weak fidelity facilitated high rewards and high risk. Weak fidelity outperformed strong fidelity in anomalous climate conditions, suggesting that the evolutionary benefits of site fidelity may be upended by increasing environmental variability. We highlight how individual behavioural specialisation may modulate the adaptive capacity of species to climate change.