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.     

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.     

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.     

Not putting all their eggs in one basket: bet‐hedging despite extraordinary annual reproductive output of desert tortoises

Bet‐hedging theory makes the counter‐intuitive prediction that, if juvenile survival is low and unpredictable, organisms should consistently reduce short‐term reproductive output to minimize the risk of reproductive failure in the long‐term. We investigated the long‐term reproductive output of an Agassiz's desert tortoise (Gopherus agassizii) population and conformance to a bet‐hedging strategy of reproduction in an unpredictable but comparatively productive environment. Most females reproduced every year, even during periods of low precipitation and poor germination of food plants, and the mean percentage of reproducing females did not differ significantly on an annual basis. Although mean annual egg production (clutch size × clutch frequency) differed significantly among years, mean clutch size and mean clutch frequency remained relatively constant. During an El Niño year, mean annual egg production and mean annual clutch frequency were the highest ever reported for this species. Annual egg production was positively influenced by maternal body size but clutch size and clutch frequency were not. Our long‐term results confirm earlier conclusions based on short‐term research that desert tortoises have a bet‐hedging strategy of producing small clutches almost every year. The risk of long‐term reproductive failure is minimized in unpredictable environments, both through time by annually producing multiple small clutches over a long reproductive lifespan, even in years of low resource availability, and through space by depositing multiple annual clutches in different locations. The extraordinary annual reproductive output of this population appears to be the result of a typically high but unpredictable biomass of annual food plants at the site relative to tortoise habitat in dryer regions. Under the comparatively productive but unpredictable conditions, tortoises conform to predictions of a bet‐hedging strategy of reproduction with relatively small but consistent clutch sizes. Published 2015. This article is a U.S. Government work and is in the public domain in the USA, Biological Journal of the Linnean Society, 2015, 115 , 399–410.     

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.     

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.     

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.     

Host‐parasite coevolution can promote the evolution of seed banking as a bet‐hedging strategy

Seed (egg) banking is a common bet‐hedging strategy maximizing the fitness of organisms facing environmental unpredictability by the delayed emergence of offspring. Yet, this condition often requires fast and drastic stochastic shifts between good and bad years. We hypothesize that the host seed banking strategy can evolve in response to coevolution with parasites because the coevolutionary cycles promote a gradually changing environment over longer times than seed persistence. We study the evolution of host germination fraction as a quantitative trait using both pairwise competition and multiple mutant competition methods, while the germination locus can be genetically linked or unlinked with the host locus under coevolution. In a gene‐for‐gene model of coevolution, hosts evolve a seed bank strategy under unstable coevolutionary cycles promoted by moderate to high costs of resistance or strong disease severity. Moreover, when assuming genetic linkage between coevolving and germination loci, the resistant genotype always evolves seed banking in contrast to susceptible hosts. Under a matching‐allele interaction, both hosts’ genotypes exhibit the same seed banking strategy irrespective of the genetic linkage between loci. We suggest host–parasite coevolution as an additional hypothesis for the evolution of seed banking as a temporal bet‐hedging strategy.     

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.     

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 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.     

Seed Germination in Desert Annuals: An Empirical Test of Adaptive Bet Hedging

Temporal variability in survivorship and reproduction is predicted to affect the evolution of life-history characters. Desert annual plants experience temporal variation in reproductive success that is largely caused by precipitation variability. We studied several populations of the desert annual Plantago insularis along a precipitation gradient. Whereas models of bet hedging in unpredictable environments generally predict one optimal germination fraction for a population, empirical studies have shown that environmental conditions during germination can cause a range of germination fractions to be expressed. In a 4-yr field study, we found that populations in historically more xeric environments had lower mean germination fractions, as is predicted by bet-hedging models. However, populations exhibited significant variation in germination among years. Two experimental studies measuring germination under several environment conditions were conducted to elucidate the source of this in situ variation. Germination fractions exhibited phenotypic plasticity in response to water availability and date within the season. Populations differed in their norms of reaction such that seeds from more xeric populations germinated under less restrictive conditions. A pattern of delayed germination consistent with among-year bet-hedging predictions arose in the field through the interaction of seed germinability and the distribution of environmental conditions during germination.     

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.     

COOPERATIVE BREEDING FAVORS MATERNAL INVESTMENT IN SIZE OVER NUMBER OF EGGS IN SPIDERS

The transition to cooperative breeding may alter maternal investment strategies depending on density of breeders, extent of reproductive skew, and allo‐maternal care. Change in optimal investment from solitary to cooperative breeding can be investigated by comparing social species with nonsocial congeners. We tested two hypotheses in a mainly semelparous system: that social, cooperative breeders, compared to subsocial, solitarily breeding congeners, (1) lay fewer and larger eggs because larger offspring compete better for limited resources and become reproducers; (2) induce egg size variation within clutches as a bet‐hedging strategy to ensure that some offspring become reproducers. Within two spider genera, Anelosimus and Stegodyphus, we compared species from similar habitats and augmented the results with a mini‐meta‐analysis of egg numbers depicted in phylogenies. We found that social species indeed laid fewer, larger eggs than subsocials, while egg size variation was low overall, giving no support for bet‐hedging. We propose that the transition to cooperative breeding selects for producing few, large offspring because reproductive skew and high density of breeders and young create competition for resources and reproduction. Convergent evolution has shaped maternal strategies similarly in phylogenetically distant species and directed cooperatively breeding spiders to invest in quality rather than quantity of offspring.     

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.     

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.     

Multitasking and the evolution of optimal clutch size in fluctuating environments

Adaptive studies of avian clutch size variation across environmental gradients have resulted in what has become known as the fecundity gradient paradox, the observation that clutch size typically decreases with increasing breeding season length along latitudinal gradients, but increases with increasing breeding season length along elevational gradients. These puzzling findings challenge the common belief that organisms should reduce their clutch size in favor of additional nesting attempts as the length of the breeding season increases, an approach typically described as a bet‐hedging strategy. Here, we propose an alternative hypothesis—the multitasking hypothesis—and show that laying smaller clutches represents a multitasking strategy of switching between breeding and recovery from breeding. Both our individual‐based and analytical models demonstrate that a small clutch size strategy is favored during shorter breeding seasons because less time and energy are wasted under the severe time constraints associated with breeding multiply within a season. Our model also shows that a within‐generation bet‐hedging strategy is not favored by natural selection, even under a high risk of predation and in long breeding seasons. Thus, saving time—wasting less time as a result of an inability to complete a breeding cycle at the end of breeding season—is likely to be the primary benefit favoring the evolution of small avian clutch sizes during short breeding seasons. We also synthesize the seasonality hypothesis (pronounced seasonality leads to larger clutch size) and clutch size‐dependent predation hypothesis (larger clutch size causes higher predation risks) within our multitasking hypothesis to develop an integrative model to help resolve the paradox of contrasting patterns of clutch size along elevational and latitudinal gradients. Ultimately, our models provide a new perspective for understanding life‐history evolution under fluctuating environments.     

Bet hedging based cooperation can limit kin selection and form a basis for mutualism

Mutualism is a mechanism of cooperation in which partners that differ help each other. As such, mutualism opposes mechanisms of kin selection and tag-based selection (for example the green beard mechanism), which are based on giving exclusive help to partners that are related or carry the same tag. In contrast to kin selection, which is a basis for parochialism and intergroup warfare, mutualism can therefore be regarded as a mechanism that drives peaceful coexistence between different groups and individuals. Here the competition between mutualism and kin (tag) selection is studied. In a model where kin selection and tag-based selection are dominant, mutualism is promoted by introducing environmental fluctuations. These fluctuations cause reduction in reproductive success by the mechanism of variance discount. The best strategy to counter variance discount is to share with agents who experience the most anticorrelated fluctuations, a strategy called bet hedging. In this way, bet hedging stimulates cooperation with the most unrelated partners, which is a basis for mutualism. Analytic results and simulations reveal that, if this effect is large enough, mutualistic strategies can dominate kin selective strategies. In addition, mutants of these mutualistic strategies that experience fluctuations that are more anticorrelated to their partner, can outcompete wild type, which can lead to the evolution of specialization. In this way, the evolutionary success of mutualistic strategies can be explained by bet hedging-based cooperation.     

Life history patterns,individual heterogeneity,and density dependence in breeding common goldeneyes of the northern boreal forest

Life history patterns and their associated tradeoffs influence population dynamics, as they determine how individuals allocate resources among competing demographic traits. Here we examined life history strategies in common goldeneyes Bucephala clangula (hereafter goldeneye), a cavity‐nesting sea duck, in the northern boreal forest of interior Alaska, USA. We used multistate capture–mark–recapture models to estimate adult survival, breeding probability, first‐year survival, and recruitment probability using a long‐term nest box study (1997–2010). We detected annual variation in adult survival, which varied from 0.74 ± 0.12 (SE) to 0.93 ± 0.06. In contrast, breeding probability remained relatively high and invariant (0.84 ± 0.11) and was positively related to individual nest success the year prior. Nonbreeding individuals in one year were more likely to remain a nonbreeder, than attempt to breed the following year. First‐year survival decreased with smaller residual duckling mass and larger brood sizes. Probability of recruitment into the breeding population conditioned on survival was constant during the study (0.96 ± 0.06), and did not vary among ages 2–5 yr‐old. Overall, goldeneyes exhibited high, but somewhat variable, adult survival, and high breeding and recruitment probabilities, which is consistent with observed patterns in bet‐hedging species that breed annually in high quality breeding environments, but whose reproductive output is often influenced by stochastic events. Demographic estimates from this study are among the first for goldeneyes within Alaska. Life history patterns are known to vary geographically, therefore, we recommend further examination of life history patterns within the distribution of goldeneyes.     

Fast life history traits promote invasion success in amphibians and reptiles

Competing theoretical models make different predictions on which life history strategies facilitate growth of small populations. While ‘fast’ strategies allow for rapid increase in population size and limit vulnerability to stochastic events, ‘slow’ strategies and bet‐hedging may reduce variance in vital rates in response to stochasticity. We test these predictions using biological invasions since founder alien populations start small, compiling the largest dataset yet of global herpetological introductions and life history traits. Using state‐of‐the‐art phylogenetic comparative methods, we show that successful invaders have fast traits, such as large and frequent clutches, at both establishment and spread stages. These results, together with recent findings in mammals and plants, support ‘fast advantage’ models and the importance of high potential population growth rate. Conversely, successful alien birds are bet‐hedgers. We propose that transient population dynamics and differences in longevity and behavioural flexibility can help reconcile apparently contrasting results across terrestrial vertebrate classes.