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.     

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.     

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.     

Bet hedging via seed banking in desert evening primroses (Oenothera, Onagraceae): demographic evidence from natural populations

Bet hedging is one solution to the problem of an unpredictably variable environment: fitness in the average environment is sacrificed in favor of lower variation in fitness if this leads to higher long-run stochastic mean fitness. While bet hedging is an important concept in evolutionary ecology, empirical evidence that it occurs is scant. Here we evaluate whether bet hedging occurs via seed banking in natural populations of two species of desert evening primroses (Oenothera, Onagraceae), one annual and one perennial. Four years of data on plants and 3 years of data on seeds yielded two transitions for the entire life cycle. One year was exceptionally dry, leading to reproductive failure in the sample areas, and the other was above average in precipitation, leading to reproductive success in four of five populations. Stochastic simulations of population growth revealed patterns indicative of bet hedging via seed banking, particularly in the annual populations: variance in fitness and fitness in the average environment were lower with seed banking than without, whereas long-run stochastic mean fitness was higher with seed banking than without across a wide range of probabilities of the wet year. This represents a novel, unusually rigorous demonstration of bet hedging from field data.     

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.     

The evolutionary ecology of seed germination of Arabidopsis thaliana: variable natural selection on germination timing

Germination timing of Arabidopsis thaliana displays strong plasticity to geographic location and seasonal conditions experienced by seeds. We identified which plastic responses were adaptive using recombinant inbred lines in a field manipulation of geographic location (Kentucky, KY; Rhode Island, RI), maternal photoperiod (14-h and 10-h days), and season of dispersal (June and November). Transgressive segregation created novel genotypes that had either higher fitness or lower fitness in certain environments than either parent. Natural selection on germination timing and its variation explained 72% of the variance in fitness among genotypes in KY, 30% in June-dispersed seeds in RI, but only 4% in November-dispersed seeds in RI. Therefore, natural selection on germination timing is an extremely efficient sieve that can determine which genotypes can persist in some locations, and its efficiency is geographically variable and depends on other aspects of life history. We found no evidence for adaptive responses to maternal photoperiod during seed maturation. We did find adaptive plasticity to season of seed dispersal in RI. Seeds dispersed in June postponed germination, which was adaptive, while seeds dispersed in November accelerated germination, which was also adaptive. We also found maladaptive plasticity to geographic location for seeds dispersed in June, such that seeds dispersed in KY germinated much sooner than the optimum time. Consequently, bet hedging in germination timing was favorable in KY; genotypes with more variation in germination timing had higher fitness because greater variation was associated with postponed germination. Selection on germination timing varied across geographic location, indicating that germination timing can be a critical stage in the establishment of genotypes in new locations. The rate of evolution of germination timing may therefore strongly influence the rate at which species can expand their range.     

Optimal germination timing in unpredictable environments: the importance of dormancy for both among‐ and within‐season variation

For organisms living in unpredictable environments, timing important life‐history events is challenging. One way to deal with uncertainty is to spread the emergence of offspring across multiple years via dormancy. However, timing of emergence is not only important among years, but also within each growing season. Here, we study the evolutionary interactions between germination strategies that deal with among‐ and within‐season uncertainty. We use a modelling approach that considers among‐season dormancy and within‐season germination phenology of annual plants as potentially independent traits and study their separate and joint evolution in a variable environment. We find that higher among‐season dormancy selects for earlier germination within the growing season. Furthermore, our results indicate that more unpredictable natural environments can counter‐intuitively select for less risk‐spreading within the season. Furthermore, strong priority effects select for earlier within‐season germination phenology which in turn increases the need for bet hedging through among‐season dormancy.     

ENVIRONMENTAL CONTROL OF SEED GERMINATION IN THLASPI ARVENSE (CRUCIFERAE)

The effect of environmental conditions during storage and imbibition on germination was investigated in field pennycress (Thlaspi arvense L.), a weed species that can behave as a winter or a summer annual. Freshly harvested seeds of an inbred line with a cold requirement for flowering exhibited primary dormancy that was rapidly lost following 1 month of afterripening in a dry state. Nondormant seeds were positively photoblastic. The light effect was mediated through phytochrome since germination was promoted by red light and inhibited by far red light. Seedling emergence was also inhibited by light filtered through a canopy of wheat leaves. Germination of field pennycress seeds was considerably more sensitive to moisture stress than two sympatric species, wild oat (Avena fatua L.) and wheat (Triticum aestivum L., cv. ERA). Seeds of the latter two species were chosen in order to compare the effect of water potential on germination in field pennycress with that in sympatric species. It was concluded that the major environmental factor limiting nondormant field pennycress seeds on the soil surface was water availability. Imbibition of fully afterripened seeds at low temperatures (6 C) induced a deep secondary dormancy. In contrast to primary dormancy, cold-induced dormancy was not alleviated by red light, alternating temperatures (21/5 C), or 2 months of dry storage at 6, 15, or 35 C. However, exogenous gibberellin A₃ or 24 weeks of dry storage resulted in germination in cold-induced dormant seeds. Secondary dormancy was not observed in fully afterripened seeds that were preincubated at 21 C for 1 or 2 days prior to the cold treatment. These results may explain the failure in field experiments to observe the cold-induced secondary dormancy that limits spring emergence in other winter annuals (J. Baskin, C. Baskin, Weed Res. 1979 19: 285–292).     

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.     

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.     

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.     

Dormancy and germination: making every seed count in restoration

From 50 to 90% of wild plant species worldwide produce seeds that are dormant upon maturity, with specific dormancy traits driven by species' occurrence geography, growth form, and genetic factors. While dormancy is a beneficial adaptation for intact natural systems, it can limit plant recruitment in restoration scenarios because seeds may take several seasons to lose dormancy and consequently show low or erratic germination. During this time, seed predation, weed competition, soil erosion, and seed viability loss can lead to plant re‐establishment failure. Understanding and considering seed dormancy and germination traits in restoration planning are thus critical to ensuring effective seed management and seed use efficiency. There are five known dormancy classes (physiological, physical, combinational, morphological, and morphophysiological), each requiring specific cues to alleviate dormancy and enable germination. The dormancy status of a seed can be determined through a series of simple steps that account for initial seed quality and assess germination across a range of environmental conditions. In this article, we outline the steps of the dormancy classification process and the various corresponding methodologies for ex situ dormancy alleviation. We also highlight the importance of record‐keeping and reporting of seed accession information (e.g. geographic coordinates of the seed collection location, cleaning and quality information, storage conditions, and dormancy testing data) to ensure that these factors are adequately considered in restoration planning.     

Seed Treatment Optimizes Benefits of Seed Bank Storage for Restoration‐Ready Seeds: The Feasibility of Prestorage Dormancy Alleviation for Mine‐Site Revegetation

Dormant seeds of 18 species from 9 families covering a diverse range of seed dormancy syndromes and life histories from the southwest Australian biodiversity hotspot were assessed for germinability following storage at 15–25°C for 36 months. A total of 10 species with physical dormancy (PY) and 8 with either physiological dormancy (PD) or morphophysiological dormancy (MPD) were assessed as part of the study. Prior to storage, germination from dormant seeds was 1–27%, rising to 41–100% following specific dormancy‐breaking treatments. When seed dormancy was removed prior to storage for 36 months seeds from all species were found to maintain a nondormant state and germinate to a similar level to that observed at the beginning of the experiment (44–100%). Likewise, seeds that did not receive a prestorage dormancy‐breaking treatment maintained a dormant state (0–50% germination) and subsequently responded well to a dormancy‐breaking treatment immediately prior to germination assessment (49–99%). There were minimal differences in response to dormancy‐breaking treatments before and after 36 months storage (average 4–6% difference) and in the germination responses observed between both storage environments assessed (15°C/15% eRH or 15–25°C air dried). Based on these findings, storing seeds in a nondormant state does not alter germinability and this approach provides significant benefits to current seed‐based restoration programs through reduction of double handling and improved seed use efficiency.     

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.     

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.     

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.     

Bet‐hedging as a mechanism for the evolution of polyandry,revisited

Females that mate with multiple males (polyandry) may reduce the risk that their eggs are fertilized by a single unsuitable male. About 25 years ago it was hypothesized that bet‐hedging could function as a mechanism favoring the evolution of polyandry, but this idea is controversial because theory indicates that bet‐hedging via polyandry can compensate the costs of mating only in small populations. Nevertheless, populations are often spatially structured, and even in the absence of spatial structure, mate‐choice opportunity can be limited to a few potential partners. We examined the effectiveness of bet‐hedging in such situations with simulations carried out under two scenarios: (1) intrinsic male quality, with offspring survival determined by male phenotype (male's ability to generate viable offspring), and (2) genetic incompatibility (offspring fitness determined nonadditively by parental genotypes). We find higher fixation probabilities for a polyandrous strategy compared to a monandrous strategy if complete reproductive failure due to male effects or parental incompatibility is pervasive in the population. Our results also indicate that bet‐hedging polyandry can delay the extinction of small demes. Our results underscore the potential for bet‐hedging to provide benefits to polyandrous females and have valuable implications for conservation biology.     

Demographic consequences of delayed germination in two annual grasses from two locations of contrasting aridity

Delayed seed germination is considered to be a bet-hedging strategy, but experimental evidence of its adaptive role as an inherited trait is still lacking. In each of two co-occuring annual grass species, populations of Mediterranean and desert origin were studied during three consecutive years for population demography and seed germination in the reciprocally introduced experimental soil seed banks. The two environments strikingly differed in productivity (annual rainfall) and predictability (variation in amount and timing of annual rainfall). The two species exhibited highly similar pattern of seed size and dormancy across the two environments. In both species, a higher proportion of dormant seeds was observed at the desert location and for the seeds of desert origin, consistent with bet-hedging buffering against unpredictability of rainfall and high probability of drought in this environment. In addition, in both species seed mass was significantly less in plants of desert origin than in plants of Mediterranean origin. The two environments differed in demographic consequences of temporal variation in precipitation. In the Mediterranean population, even in the year of least precipitation, adults grew to maturity and seeds were produced. These seeds served to maintain population size. In contrast, in the desert population, in the year of least rainfall no seedlings survived to maturity and the soil seed bank was the only source of population persistence. Altogether, the results concur with predicted by adaptive bet hedging importance of delayed germination under marginal precipitation.     

Should mothers provision their offspring equally? A manipulative field test

Within‐brood variation in offspring size is universal, but its causes are unclear. Theoretical explanations for within‐brood variation commonly invoke bet‐hedging, although alternatives consider the role of sibling competition. Despite abundant theory, empirical manipulations of within‐brood variation in offspring size are rare. Using a field experiment, we investigate the consequences of unequal maternal provisioning for both maternal and offspring fitness in a marine invertebrate. We create experimental broods of siblings with identical mean, but different variance, in offspring size, and different sibling densities. Overall, more‐variable broods had higher mean performance than less‐variable broods, suggesting benefits of unequal provisioning that arise independently of bet‐hedging. Complementarity effects drove these benefits, apparently because offspring‐size variation promotes resource partitioning. We suggest that when siblings compete for the same resources, and offspring size affects niche usage, the production of more‐variable broods can provide greater fitness returns given the same maternal investment; a process unanticipated by the current theory.