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.     

Bet hedging in desert winter annual plants: optimal germination strategies in a variable environment

In bet hedging, organisms sacrifice short‐term success to reduce the long‐term variance in success. Delayed germination is the classic example of bet hedging, in which a fraction of seeds remain dormant as a hedge against the risk of complete reproductive failure. Here, we investigate the adaptive nature of delayed germination as a bet hedging strategy using long‐term demographic data on Sonoran Desert winter annual plants. Using stochastic population models, we estimate fitness as a function of delayed germination and identify evolutionarily stable strategies for 12 abundant species in the community. Results indicate that delayed germination meets the criteria as a bet hedging strategy for all species. Density‐dependent models, but not density‐independent ones, predicted optimal germination strategies that correspond remarkably well with observed patterns. By incorporating naturally occurring variation in seed and seedling dynamics, our results present a rigorous test of bet hedging theory within the relevant environmental context.     

Spatially heterogeneous stochasticity and the adaptive diversification of dormancy

Diversified bet‐hedging, a strategy that leads several individuals with the same genotype to express distinct phenotypes in a given generation, is now well established as a common evolutionary response to environmental stochasticity. Life‐history traits defined as diversified bet‐hedging (e.g. germination or diapause strategies) display marked differences between populations in spatial proximity. In order to find out whether such differences can be explained by local adaptations to spatially heterogeneous environmental stochasticity, we explored the evolution of bet‐hedging dormancy strategies in a metapopulation using a two‐patch model with patch differences in stochastic juvenile survival. We found that spatial differences in the level of environmental stochasticity, restricted dispersal, increased fragmentation and intermediate survival during dormancy all favour the adaptive diversification of bet‐hedging dormancy strategies. Density dependency also plays a major role in the diversification of dormancy strategies because: (i) it may interact locally with environmental stochasticity and amplify its effects; however, (ii) it can also generate chaotic population dynamics that may impede diversification. Our work proposes new hypotheses to explain the spatial patterns of bet‐hedging strategies that we hope will encourage new empirical studies of this topic.     

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.     

When sensing is gambling: An experimental system reveals how plasticity can generate tunable bet‐hedging strategies

Genotypes can persist in unpredictable environments by “hedging their bets” and producing diverse phenotypes. Theoretical studies have shown that the phenotypic variability needed for a bet‐hedging strategy can be generated by factors either inside or outside an organism. However, sensing the environment and bet hedging are frequently treated as distinct evolutionary strategies. Furthermore, nearly all empirical studies of the molecular underpinnings of bet‐hedging strategies to date have focused on internal sources of variability. We took a synthetic approach and constructed an experimental system where a phenotypic trade‐off is mediated by actively sensing a cue present in the environment. We show that active sensing can generate a diversified bet‐hedging strategy. Mutations affecting the norm of reaction to the cue alter the diversification strategy, indicating that bet hedging by active sensing is evolvable. Our results indicate that a broader class of biological systems should be considered as potential examples of bet‐hedging strategies, and that research into the structure of environmental variability is needed to distinguish bet‐hedging strategies from adaptive plasticity.     

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.     

Contact‐dependent growth inhibition induces high levels of antibiotic‐tolerant persister cells in clonal bacterial populations

Bacterial populations can use bet‐hedging strategies to cope with rapidly changing environments. One example is non‐growing cells in clonal bacterial populations that are able to persist antibiotic treatment. Previous studies suggest that persisters arise in bacterial populations either stochastically through variation in levels of global signalling molecules between individual cells, or in response to various stresses. Here, we show that toxins used in contact‐dependent growth inhibition (CDI) create persisters upon direct contact with cells lacking sufficient levels of CdiI immunity protein, which would otherwise bind to and neutralize toxin activity. CDI‐mediated persisters form through a feedforward cycle where the toxic activity of the CdiA toxin increases cellular (p)ppGpp levels, which results in Lon‐mediated degradation of the immunity protein and more free toxin. Thus, CDI systems mediate a population density‐dependent bet‐hedging strategy, where the fraction of non‐growing cells is increased only when there are many cells of the same genotype. This may be one of the mechanisms of how CDI systems increase the fitness of their hosts.     

Weak breeding seasonality of a songbird in a seasonally arid tropical environment arises from individual flexibility and strongly seasonal moult

In some tropical birds, breeding seasonality is weak at the population level, even where there are predictable seasonal peaks in environmental conditions. It therefore remains unclear whether individuals are adapted to breeding at specific times of the year or flexible to variable environmental conditions. We tested whether the relative year‐round breeding activity of the Common Bulbul Pycnonotus barbatus arises due to within‐individual variability in breeding dates. We collected data from 827 birds via mist‐netting over 2 years with corresponding local weather data. We used a combination of climate envelope and generalized linear mixed models to explore how the timing of breeding is influenced by time of year, individual variation, rainfall and temperature in a West African savannah where seasonal precipitation determines annual variation in environmental conditions. We also pooled 65 breeding records from 19 individuals recorded between 2006 and 2017 based on brood patch occurrence and behavioural observation to compare within‐individual and population variability in breeding dates. We show that the breeding dates of individuals may be as variable as for the population as a whole. However, we observed a seasonal peak in juvenile occurrence that varies significantly between years. Models suggest no relationship between nesting and moult, and within‐year variation in rainfall and temperature, and birds were unlikely to breed during moult but may do so afterwards. Moult was very seasonal, correlating strongly with day length. We suggest that because environmental conditions permit year‐round breeding, and because reproductive output is subject to high predation risk, there is probably a weak selection for individuals to match breeding with variable peak conditions in the environment. Instead, moult, which always occurs annually and successfully, is probably under strong selection to match variable peak conditions in the environment so that long‐term survival ensures future reproduction.     

Bet hedging or not? A guide to proper classification of microbial survival strategies

Bacteria have developed an impressive ability to survive and propagate in highly diverse and changing environments by evolving phenotypic heterogeneity. Phenotypic heterogeneity ensures that a subpopulation is well prepared for environmental changes. The expression bet hedging is commonly (but often incorrectly) used by molecular biologists to describe any observed phenotypic heterogeneity. In evolutionary biology, however, bet hedging denotes a risk-spreading strategy displayed by isogenic populations that evolved in unpredictably changing environments. Opposed to other survival strategies, bet hedging evolves because the selection environment changes and favours different phenotypes at different times. Consequently, in bet hedging populations all phenotypes perform differently well at any time, depending on the selection pressures present. Moreover, bet hedging is the only strategy in which temporal variance of offspring numbers per individual is minimized. Our paper aims to provide a guide for the correct use of the term bet hedging in molecular biology.     

Joint optimal ordering and weather hedging decisions: mean-CVaR model

This paper considers the problem of hedging inventory risk for a seasonal product whose demand is sensitive to weather conditions, such as the average seasonal temperature. The newsvendor not only decides the order quantity, but also adopts a weather hedging strategy. A typical hedging strategy is to use an option (weather derivative) that is constructed on a weather index before the season begins, which will compensate the buyer of the option if the actual seasonal weather index is above (or below) a given strike level. We adopt the risk measure of Conditional-Value at Risk ( $\hbox{CVaR}$ ) and explore the joint decision problem in mean-CVaR criterion. We find that the weather derivative hedging can increase order quantity. Furthermore, it can help the risk-averse newsvendor improve both expected overall and downside profits.     

Seasonal genetic variation associated with population dynamics of a poecilogonous polychaete worm

Poecilogonous species show variation in developmental mode, with larvae that differ both morphologically and ecologically. The spionid polychaete Pygospio elegans shows variation in developmental mode not only between populations, but also seasonally within populations. We investigated the consequences of this developmental polymorphism on the spatial and seasonal genetic structure of P. elegans at four sites in the Danish Isefjord‐Roskilde‐Fjord estuary at six time points, from March 2014 until February 2015. We found genetic differentiation between our sampling sites as well as seasonal differentiation at two of the sites. The seasonal genetic shift correlated with the appearance of new size cohorts in the populations. Additionally, we found that the genetic composition of reproductive individuals did not always reflect the genetic composition of the entire sample, indicating that variance in reproductive success among individuals is a likely explanation for the patterns of chaotic genetic patchiness observed during this and previous studies. The heterogeneous, unpredictable character of the estuary might maintain poecilogony in P. elegans as a bet‐hedging strategy in the Isefjord‐Roskilde‐Fjord complex in comparison with other sites where P. elegans are expected to be fixed to a certain mode of development.     

Within‐and among‐year germination in Sonoran Desert winter annuals: bet hedging and predictive germination in a variable environment

In variable environments, organisms must have strategies to ensure fitness as conditions change. For plants, germination can time emergence with favourable conditions for later growth and reproduction (predictive germination), spread the risk of unfavourable conditions (bet hedging) or both (integrated strategies). Here we explored the adaptive value of within‐ and among‐year germination timing for 12 species of Sonoran Desert winter annual plants. We parameterised models with long‐term demographic data to predict optimal germination fractions and compared them to observed germination. At both temporal scales we found that bet hedging is beneficial and that predicted optimal strategies corresponded well with observed germination. We also found substantial fitness benefits to varying germination timing, suggesting some degree of predictive germination in nature. However, predictive germination was imperfect, calling for some degree of bet hedging. Together, our results suggest that desert winter annuals have integrated strategies combining both predictive plasticity and bet hedging.     

Linking behavioral thermoregulation,boldness, and individual state in male Carpetan rock lizards

Mechanisms affecting consistent interindividual behavioral variation (i.e., animal personality) are of wide scientific interest. In poikilotherms, ambient temperature is one of the most important environmental factors with a direct link to a variety of fitness‐related traits. Recent empirical evidence suggests that individual differences in boldness are linked to behavioral thermoregulation strategy in heliothermic species, as individuals are regularly exposed to predators during basking. Here, we tested for links between behavioral thermoregulation strategy, boldness, and individual state in adult males of the high‐mountain Carpetan rock lizard (Iberolacerta cyreni). Principal component analysis revealed the following latent links in our data: (i) a positive relationship of activity with relative limb length and color brightness (PC1, 23% variation explained), (ii) a negative relationship of thermoregulatory precision with parasite load and risk‐taking (PC2, 20.98% variation explained), and (iii) a negative relationship between preferred body temperature and relative limb length (PC3, 19.23% variation explained). We conclude that differences in boldness and behavioral thermoregulatory strategy could be explained by both stable and labile state variables. The moderate link between behavioral thermoregulatory strategy and risk‐taking personality in our system is plausibly the result of differences in reproductive state of individuals or variation in ecological conditions during the breeding season.     

Bet hedging in a warming ocean: predictability of maternal environment shapes offspring size variation in marine sticklebacks

Bet hedging at reproduction is expected to evolve when mothers are exposed to unpredictable cues for future environmental conditions, whereas transgenerational plasticity (TGP) should be favoured when cues reliably predict the environment offspring will experience. Since climate predictions forecast an increase in both temperature and climate variability, both TGP and bet hedging are likely to become important strategies to mediate climate change effects. Here, the potential to produce variably sized offspring in both warming and unpredictable environments was tested by investigating whether stickleback (Gasterosteus aculeatus) mothers adjusted mean offspring size and within‐clutch variation in offspring size in response to experimental manipulation of maternal thermal environment and predictability (alternating between ambient and elevated water temperatures). Reproductive output traits of F1 females were influenced by both temperature and environmental predictability. Mothers that developed at ambient temperature (17 °C) produced larger, but fewer eggs than mothers that developed at elevated temperature (21 °C), implying selection for different‐sized offspring in different environments. Mothers in unpredictable environments had smaller mean egg sizes and tended to have greater within‐female egg size variability, especially at 21 °C, suggesting that mothers may have dynamically modified the variance in offspring size to spread the risk of incorrectly predicting future environmental conditions. Both TGP and diversification influenced F2 offspring body size. F2 offspring reared at 21 °C had larger mean body sizes if their mother developed at 21 °C, but this TGP benefit was not present for offspring of 17 °C mothers reared at 17 °C, indicating that maternal TGP will be highly relevant for ocean warming scenarios in this system. Offspring of variable environment mothers were smaller but more variable in size than offspring from constant environment mothers, particularly at 21 °C. In summary, stickleback mothers may have used both TGP and diversified bet‐hedging strategies to cope with the dual stress of ocean warming and environmental uncertainty.     

Bet‐hedging as a complex interaction among developmental instability,environmental heterogeneity,dispersal, and life‐history strategy

One potential evolutionary response to environmental heterogeneity is the production of randomly variable offspring through developmental instability, a type of bet‐hedging. I used an individual‐based, genetically explicit model to examine the evolution of developmental instability. The model considered both temporal and spatial heterogeneity alone and in combination, the effect of migration pattern (stepping stone vs. island), and life‐history strategy. I confirmed that temporal heterogeneity alone requires a threshold amount of variation to select for a substantial amount of developmental instability. For spatial heterogeneity only, the response to selection on developmental instability depended on the life‐history strategy and the form and pattern of dispersal with the greatest response for island migration when selection occurred before dispersal. Both spatial and temporal variation alone select for similar amounts of instability, but in combination resulted in substantially more instability than either alone. Local adaptation traded off against bet‐hedging, but not in a simple linear fashion. I found higher‐order interactions between life‐history patterns, dispersal rates, dispersal patterns, and environmental heterogeneity that are not explainable by simple intuition. We need additional modeling efforts to understand these interactions and empirical tests that explicitly account for all of these factors.     

Offspring polymorphism and bet hedging: a large‐scale,phylogenetic analysis

Offspring polymorphism is a reproductive strategy where individual organisms simultaneously produce offspring that differ in morphology and ecology. It occurs across the Tree of Life but is particularly common among plants, where it is termed seed (diaspore) heteromorphism. The prevalence of this strategy in unpredictably varying environments has resulted in the assumption that it serves as a bet‐hedging mechanism. We found 101 examples of this strategy in southwestern North America. We provide phylogenetically informed evidence for the hypothesis that the occurrence of seed heteromorphism increases with increasing environmental variability, though this pattern was only significant for aridity, one of our two rainfall variability metrics. We provide a strong test of bet hedging for a large, taxonomically diverse set of seed heteromorphic species, lending support to the hypothesis that bet hedging is an important mechanistic driver for the evolution of seed heteromorphism.     

CLINAL VARIATION IN SEED TRAITS INFLUENCING LIFE CYCLE TIMING IN ARABIDOPSIS THALIANA

Early life‐history transitions are crucial determinants of lifetime survival and fecundity. Adaptive evolution in early life‐history traits involves a complex interplay between the developing plant and its current and future environments. We examined the plant's earliest life‐history traits, dissecting an integrated suite of pregermination processes: primary dormancy, thermal induction of secondary dormancy, and seasonal germination response. We examined genetic variation in the three processes, genetic correlations among the processes, and the scaling of germination phenology with the source populations’ climates. A spring annual life history was associated with genetic propensities toward both strong primary dormancy and heat‐induced secondary dormancy, alone or in combination. Lineages with similar proportions of winter and spring annual life history have both weak primary dormancy and weak thermal dormancy induction. A genetic bias to adopt a spring annual strategy, mediated by rapid loss of primary dormancy and high thermal dormancy induction, is associated with a climatic gradient characterized by increasing temperature in summer and rainfall in winter. This study highlights the importance of considering combinations of multiple genetically based traits along a climatic gradient as adaptive strategies differentiating annual plant life‐history strategies. Despite the genetic‐climatic cline, there is polymorphism for life‐history strategies within populations, classically interpreted as bet hedging in an unpredictable world.     

Differences in prey personality mediate trophic cascades

Functional trait approaches in ecology chiefly assume the mean trait value of a population adequately predicts the outcome of species interactions. Yet this assumption ignores substantial trait variation among individuals within a population, which can have a profound effect on community structure and function. We explored individual trait variation through the lens of animal personality to test whether among‐individual variation in prey behavior mediates trophic interactions. We quantified the structure of personalities within a population of generalist grasshoppers and examined, through a number of field and laboratory‐based experiments, how personality types could impact tri‐trophic interactions in a food chain. Unlike other studies of this nature, we used spatial habitat domains to evaluate how personality types mechanistically map to behaviors relevant in predator–prey dynamics and found shy and bold individuals differed in both their habitat use and foraging strategy under predation risk by a sit‐and‐wait spider predator. In the field‐based mesocosm portion of our study, we found experimental populations of personality types differed in their trophic impact, demonstrating that prey personality can mediate trophic cascades. We found no differences in respiration rates or body size between personality types used in the mesocosm experiment, indicating relative differences in trophic impact were not due to variation in prey physiology but rather variation in behavioral strategies. Our work demonstrates how embracing the complexity of individual trait variation can offer mechanistically richer understanding of the processes underlying trophic interactions.     

A tree in the eyes of a moth – temporal variation in oak leaf quality and leaf-miner performance

When examined at any moment in time, different parts of an individual oak tree exhibit almost as large differences in quality as different trees. But how consistent are such patterns in time? In this paper, we use intraclass correlations to assess the temporal consistency of host plant quality at several spatial scales. As measures of quality, we use both individual chemical attributes (phenolic contents) and the overall performance (larval survival) of the host‐specific leaf‐miner Tischeria ekebladella. Concentrations of 24 phenolic compounds were monitored on seven trees throughout a season. Variation in mine initiation and larval survival rates was assessed for individuals transplanted to another set of trees early versus later in the season, while year‐to‐year variation in larval survival was studied through stratified surveys of wild individuals during three years. At all time scales considered, measures of host quality were moderately consistent: a tree favourable in quality at one point in time often remained so, but there was abundant variation around this relationship (ρ=0.4–0.6). One hierarchical level deviated from this general pattern: on individual branches, larval survival rates varied randomly among years (ρ=0). Our study suggests that the quality of trees, and in particular of smaller units within trees, may be difficult to predict both in space and in time. To account for this, insects might benefit from adopting a bet‐hedging strategy when selecting resources.