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.     

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.     

Playing smart vs. playing safe: the joint expression of phenotypic plasticity and potential bet hedging across and within thermal environments

Adaptive phenotypic plasticity evolves when cues reliably predict fitness consequences of life‐history decisions, whereas bet hedging evolves when environments are unpredictable. These modes of response should be jointly expressed, because environmental variance is composed of both predictable and unpredictable components. However, little attention has been paid to the joint expression of plasticity and bet hedging. Here, I examine the simultaneous expression of plasticity in germination rate and two potential bet‐hedging traits – germination fraction and within‐season diversification in timing of germination – in seeds from multiple seed families of five geographically distant populations of Lobelia inflata (L.) subjected to a thermal gradient. Populations differ in germination plasticity to temperature, in total germination fraction and in the expression of potential diversification in the timing of germination. The observation of a negative partial correlation between the expression of plasticity and germination variance (potential diversification), and a positive correlation between plasticity and germination fraction is suggestive of a trade‐off between modes of response to environmental variance. If the observed correlations are indicative of those between adaptive plasticity and bet hedging, we expect an optimal balance to exist and differ among populations. I discuss the challenges involved in testing whether the balance between plasticity and bet hedging depends on the relative predictability of environmental variance.     

Frequency‐dependent selection: a diversifying force in microbial populations

The benefits of “bet‐hedging” strategies have been assumed to be the main cause of phenotypic diversity in biological populations. However, in their recent work, Healey et al ( 2016 ) provide experimental support for negative frequency‐dependent selection (NFDS) as an alternative driving force of diversity. NFDS favors rare phenotypes over common ones, resulting in an evolutionarily stable mixture of phenotypes that is not necessarily optimal for population growth.     

Low‐molecular weight carbohydrates modulate dormancy and are required for post‐germination growth in turions of Spirodela polyrhiza

The aquatic duckweed Spirodela polyrhiza propagates itself vegetatively by forming turions – bud‐like perennation organs – in the autumn, which spend the winter on the bottom of ponds and then germinate in the following spring and proliferate on the water surface. Newly formed turions usually require a period of cold after‐ripening and light to germinate effectively, but an ample supply of exogenous sugar can lead to germination even in the dark and independent of after‐ripening. The results of the present study indicate that the availability of readily metabolised carbohydrates is a determining factor for turion germination. Freshly harvested turions do not contain soluble, low‐molecular weight carbohydrates at a level sufficient to allow germination to take place, but after‐ripened turions do. Augmentation of the soluble carbohydrate content during after‐ripening derives from gradual breakdown of reserve starch of the turions. The long time required for any germination to be observed in turions incubated in darkness and the limited frequency of germination in the dark (about 50% of turion population), even with an ample external sugar, supply emphasise that both after‐ripening and light are essential for ensuring rapid germination and subsequent frond proliferation at an ecologically appropriate time. The carbohydrate supply required for rapid proliferation of the fronds produced at germination is provided by the rapid light‐induced breakdown of turion reserve starch.     

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.     

Interaction of maternal environment and allelic differences in seed vigour genes determines seed performance in Brassica oleracea

Seed vigour is a key trait essential for the production of sustainable and profitable crops. The genetic basis of variation in seed vigour has recently been determined in Brassica oleracea, but the relative importance of the interaction with parental environment is unknown. We produced seeds under a range of maternal environments, including global warming scenarios. Lines were compared that had the same genetic background, but different alleles (for high and low vigour) at the quantitative trait loci responsible for determining seed vigour by altering abscisic acid (ABA) content and sensitivity. We found a consistent effect of beneficial alleles across production environments; however, environmental stress during production also had a large impact that enhanced the genetic difference in seed performance, measured as germination speed, resistance to controlled deterioration and induction of secondary dormancy. Environmental interaction with allelic differences in key genes that determine ABA content and sensitivity develops a continuity in performance from rapid germination through to failure to complete germination, and increasing depths of seed dormancy. The genetic–environmental interaction revealed provides a robust mechanism of bet‐hedging to minimize environmental risk during subsequent germination, and this could have facilitated the rapid change in seed behaviour (reduced dormancy and rapid germination) observed during crop domestication.     

Repeated evolution of terrestrial lineages in a continental lizard radiation

The “early‐burst” model of adaptive radiation predicts an early increase in phenotypic disparity concurrent with lineage diversification. Although most studies report a lack of this coupled pattern, the underlying processes are not identified. The continental radiation of Hemidactylus geckos from Peninsular India includes morphologically diverse species that occupy various microhabitats. This radiation began diversifying ~36 Mya with an early increase in lineage diversification. Here, we test the “early‐burst” hypothesis by investigating the presence of ecomorphs and examining the pattern of morphological diversification in a phylogenetic framework. Two ecomorphs—terrestrial and scansorial species—that vary significantly in body size and toepad size were identified. Unlike the prediction of the “early‐burst” model, we find that disparity in toepad morphology accumulated more recently ~14 Mya and fit the Ornstein‐Ulhenbeck model. Ancestral state reconstruction of the two ecomorphs demonstrates that terrestrial lineages evolved independently at least five times from scansorial ancestors, with the earliest diversification in terrestrial lineages 19–12 Mya. Our study demonstrates a delayed increase in morphological disparity as a result of the evolution of terrestrial ecomorphs. The diversification of terrestrial lineages is concurrent with the establishment of open habitat and grasslands in Peninsular India, suggesting that the appearance of this novel resource led to the adaptive diversification.     

Differences in developmental strategies between long‐settled and invasion‐front populations of the cane toad in Australia

Phenotypic plasticity can enhance a species’ ability to persist in a new and stressful environment, so that reaction norms are expected to evolve as organisms encounter novel environments. Biological invasions provide a robust system to investigate such changes. We measured the rates of early growth and development in tadpoles of invasive cane toads (Rhinella marina) in Australia, from a range of locations and at different larval densities. Populations in long‐colonized areas have had the opportunity to adapt to local conditions, whereas at the expanding range edge, the invader is likely to encounter challenges that are both novel and unpredictable. We thus expected invasion‐vanguard populations to exhibit less phenotypic plasticity than range‐core populations. Compared to clutches from long‐colonized areas, clutches from the invasion front were indeed less plastic (i.e. rates of larval growth and development were less sensitive to density). In contrast, those rates were highly variable in clutches from the invasion front, even among siblings from the same clutch under standard conditions. Clutches with highly variable rates of growth and development under constant conditions had lower phenotypic plasticity, suggesting a trade‐off between these two strategies. Although these results reveal a strong pattern, further investigation is needed to determine whether these different developmental strategies are adaptive (i.e. adaptive phenotypic plasticity vs. bet‐hedging) or instead are driven by geographic variation in genetic quality or parental effects.     

Obligate annual and successive facultative diapause establish a bet‐hedging strategy of Rhagoletis cerasi (Diptera: Tephritidae) in seasonally unpredictable environments

To cope with temporal and spatial heterogeneity of habitats, herbivorous insects in the temperate zone usually enter diapause that facilitates synchronization of their life cycle with specific stages of host plants, such as fruit ripening. In the present study, we address those factors regulating dormancy responses as part of a ‘longer strategy’ to persist and thrive in temperate environments, focusing on Rhagoletis cerasi, a univoltine, oligophagous species, which overwinters as pupae and emerges when host fruits are available for oviposition at local scale. To ensure population survival and reproduction at habitats with ecological heterogeneity, R. cerasi has evolved a sophisticated diapause strategy based on a combination of local adaptation and diversified bet‐hedging strategies. Diapause duration is determined both by (i) the adaptive response to local host fruit phenology patterns (annual diapause) and (ii) the plastic responses to unpredictable inter‐annual (temporal) climatic variability that drives a proportion of the populations to extend dormancy by entering a second, successive, facultative cycle of prolonged diapause as part of a bet‐hedging strategy. Besides the dormant periods, post‐diapause development (which varies among populations) exerts ‘fine tune’ adjustments that assure synchronization and may correct possible errors. Adults emerging from pupae with prolonged diapause are larger in body size compared with counterparts emerging during the first year of diapause. However, female fecundity rates are reduced, followed by an extended post‐oviposition period, whereas adult longevity remains unaffected. Overall, it appears that R. cerasi populations are adapted to ecological conditions of local habitats and respond plastically to unpredictable environmental (climatic) conditions.     

Variability in thermal and phototactic preferences in Drosophila may reflect an adaptive bet‐hedging strategy

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.     

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.     

Early and late developmental arrest as complementary embryonic bet‐hedging strategies in African killifish

The production of dormant eggs is a crucial adaptation for African killifish of the genus Nothobranchius to survive in temporary waters. These habitats are often characterized by unpredictable variation in the suitability of growing seasons as a result of variable lengths of inundations and temporary colonization by piscivorous fish. Incomplete hatching could enable killifish to buffer against reproductive failure during unsuitable inundations. Although this phenomenon has been tentatively linked to variation in dormancy states, it has never been investigated under controlled conditions and its viability as a bet hedging strategy to distribute offspring over several inundations remains unclear. In the present study, we used common garden experiments to assess the contribution of environmental modulation and bet hedging to delayed hatching in Nothobranchius killifish by testing the feasibility of arrested development in the presence and absence of environmental cues. Overall, the results confirmed that the presence of cues signalling a threat (predator kairomones) inhibited hatching. However, delayed development also occurred independent of cues and was regulated at two stages. Developmental arrest in energy‐efficient dormancy stages could present a means for long‐term bet hedging over years, whereas arrest in the energy‐consuming final stage may serve a similar purpose over shorter time scales. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 941–948.     

Diapause termination of Rhagoletis cerasi pupae is regulated by local adaptation and phenotypic plasticity: escape in time through bet‐hedging strategies

Persistence and thriving of univoltine, herbivore insect species of the temperate zone rely on obligate diapause response that ensures winter survival and synchronization with host phenology. We used a stenophagous fruit fly (Rhagoletis cerasi) with obligate pupae diapause to determine genetic and environmental effects on diapause intensity of geographically isolated populations with habitat heterogeneity. Pupae from two Greek and one German populations with various gene flow rates were exposed at five constant chilling temperatures (0–12 °C) for different durations and then incubated at a high temperature until all adults have emerged. Pupae diapause intensity differs among Greek and German populations, suggesting an adaptive response to habitat heterogeneity (mostly differences in phenology patterns of local host cultivars). Moderately warm winter temperatures, such as 8 °C, promote diapause termination in all three populations. Insufficient chilling (short duration or warmer temperatures) regulates the expression of prolonged dormancy. Interestingly, extended chilling (longer than required for terminating diapause) ‘return’ pupae to another (facultative) cycle of dormancy enabling adults to emerge during the next appropriate ‘window of time’; a strategy first time reported for univoltine insects. Consequently, diapause duration of R. cerasi is determined both by i) the adaptive response to local climatic conditions (annual dormancy) and ii) the plastic responses to interannual climatic variability resulting in two types of long life cycles within populations, prolonged and facultative dormancy as response to insufficient chilling and extended exposure to chilling, respectively. Long life cycles are expressed as a part of dormancy bet‐hedging strategies of R. cerasi populations.     

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.     

Bet‐hedging germination in annual plants: a sound empirical test of the theoretical foundations

Seed dormancy is thought to be a key mechanism allowing annual plants to spread extinction risk in unpredictably varying environments. Theory predicts increasing germination fractions with increasing probability of reproductive success but solid empirical evidence is scarce and often confounded with environmental factors. Here we provide an empirical test of bet‐hedging via delayed germination for three annual plant species along a ‘predictability gradient’ in Israel. We excluded confounding environmental and maternal effects by raising inbred seed families and germinating them under controlled conditions. Additionally, we germinated field‐collected seeds in three consecutive seasons to compare their germination with inbred families where maternal effects were removed. Risk of reproductive failure was quantified using demographic data from the field and from second‐generation inbred lines raised in a rainfall gradient in the greenhouse. Our findings were consistent with bet‐hedging theory in that germination fraction was negatively related to species‐ and site‐specific risk of reproductive failure. Both field and hand‐raised seeds of one species exhibited higher dormancy with increasing risk of reproductive failure across sites, and hand‐raised seeds of another species showed the same pattern. The third species exhibited a rather random pattern of germination between years and sites, corresponding to the lack of site‐specific risk of reproductive failure. Species‐specific patterns of dormancy and risk could be related to alternative risk‐spreading strategies such as high adult survival, but were also affected by phylogeny. We provide strong empirical evidence for seed dormancy being a mechanism to reduce the risk of reproductive failure in highly variable environments, but a larger number of rigorous experimental tests of bet hedging germination are needed. Specifically, the genetic basis of bet‐hedging must be shown in species with different life histories, for demonstrating that dormancy is adaptive and how it is modified by other risk‐spreading traits.     

Germination of Spirodela polyrhiza turions: the role of culture conditions during turion development

The rapidly germinating "old" turions of Spirodela polyrhizawere shown to derive mainly from the slowly germinating "young"turions. This modification to "old" turions could occur evenin isolated "young" turions, and was accelerated by sucrose.It is suggested that this modification is a form of turion senescenceand that turion initiation and maturation are strongly influencedby exogenous carbon and nitrogen sources. (Received November 19, 1979; )     

Reversible non‐genetic phenotypic heterogeneity in bacterial quorum sensing

Bacteria co‐ordinate their social behaviour in a density‐dependent manner by production of diffusible signal molecules by a process known as quorum sensing (QS). It is generally assumed that in homogenous environments and at high cell density, QS synchronizes cells in the population to perform collective social tasks in unison which maximize the benefit at the inclusive fitness of individuals. However, evolutionary theory predicts that maintaining phenotypic heterogeneity in performing social tasks is advantageous as it can serve as a bet‐hedging survival strategy. Using Pseudomonas syringae and Xanthomonas campestris as model organisms, which use two diverse classes of QS signals, we show that two distinct subpopulations of QS‐responsive and non‐responsive cells exist in the QS‐activated population. Addition of excess exogenous QS signal does not significantly alter the distribution of QS‐responsive and non‐responsive cells in the population. We further show that progeny of cells derived from these subpopulations also exhibited heterogeneous distribution patterns similar to their respective parental strains. Overall, these results support the model that bacteria maintain QS‐responsive and non‐responsive subpopulations at high cell densities in a bet‐hedging strategy to simultaneously perform functions that are both positively and negatively regulated by QS to improve their fitness in fluctuating environments.     

Maternal age and spine development in the rotifer Brachionus calyciflorus: increase of spine length with birth orders1

1. Maternal effects have long been known to influence phenotypic plasticity in rotifers. Females in Brachionus calyciflorus and several other species produce long‐spined offspring when the predatory rotifer Asplanchna is present; B. calyciflorus also develops short spines when food concentrations are low. These spines protect against predation and decrease food threshold concentrations. 2. Some strains of B. calyciflorus develop long spines even in the absence of Asplanchna and other environmental stimuli. We demonstrate in this study that spine length in such cases is dependent on the age of the mother. 3. In strains from Florida and Georgia, offspring spine length increased significantly with birth order, sometimes to lengths formerly observed only in the presence of Asplanchna. Significant variation in this trait was found among and within clones of a strain. Offspring body size also increased with maternal age. This is the first time maternal age has been shown to affect rotifer morphology. 4. These birth‐order effects may have important ecological implications and explain phenotypic plasticity and polymorphism in body size and spine length in populations when predators are absent and food concentrations are high. They may be a bet‐hedging mechanism to assure adaptation to rapid changes in predation pressure or food conditions.