Uncertainty is a problem not only in human decision-making, but is a prevalent quality of natural environments and thus requires evolutionary response. Unpredictable natural selection is expected to result in the evolution of bet-hedging strategies, which are adaptations to long-term fluctuating selection. Despite a recent surge of interest in bet hedging, its study remains mired in conceptual and practical difficulties, compounded by confusion over what constitutes evidence for its existence. Here, I attempt to resolve misunderstandings about bet hedging and its relationship with other modes of response to environmental change, identify the challenges inherent to its study and assess the state of existing empirical evidence. The variety and distribution of plausible bet-hedging traits found across 16 phyla in over 100 studies suggest their ubiquity. Thus, bet hedging should be considered a specific mode of response to environmental change. However, the distribution of bet-hedging studies across evidence categoriesdefined according to potential strength-is heavily skewed towards weaker categories, underscoring the need for direct appraisals of the adaptive significance of putative bet-hedging traits in nature.

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Natural environments are characterized by unpredictability over all time scales. This stochasticity is expected on theoretical grounds to result in the evolution of 'bet-hedging' traits that maximize the long term, or geometric mean fitness even though such traits do not maximize fitness over shorter time scales. The geometric mean principle is thus central to our interpretation of optimality and adaptation; however, quantitative empirical support for bet hedging is lacking. Here, I report a quantitative test using the timing of seed germination-a model diversification bet-hedging trait-in Lobelia inflata under field conditions. In a phenotypic manipulation study, I find the magnitude of fluctuating selection acting on seed germination timing-across 70 intervals throughout five seasons-to be extreme: fitness functions for survival are complex and multimodal within seasons and significantly dissimilar among seasons. I confirm that the observed magnitude of fluctuating selection is sufficient to account for the degree of diversification behaviour characteristic of individuals of this species. The geometric mean principle has been known to economic theory for over two centuries; this study now provides a quantitative test of optimality of a bet-hedging trait in nature.

Seed germination constitutes an important event in the life cycle of plants. Two related seed traits affect fitness: seed size and the timing of seed germination. In three sets of experiments, we (1) partition the sources of seed-size variance in Lobelia inflata into components attributable to fruit size, relative fruit position, and parental identity; (2) examine the influence of pregermination conditions and seed size on time to germination; and (3) assess the fitness consequences of seed size and germination timing under seminatural, harsh conditions. Seed-size variance is attributable to both parental identity and fruit position within an individual. Distal fruits produce larger but fewer seeds. No significant correlation exists between fruit size and seed size, but a trade-off is found between the number and size of seeds contained in a fruit after correcting for fruit size. The timing of germination is influenced by seed size, light conditions before winter, and winter duration. Germination timing influences survival, and despite small seed size in this species (2 × 10 g/seed), seed size has a persistent and significant association with both final plant size and the probability of survival to autumn.

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.

Abstract. Environmental variation that is not predictably related to cues is expected to drive the evolution of bethedging strategies. The high variance observed in the timing of seed germination has led to it being the most cited diversification strategy in the theoretical bet-hedging literature. Despite this theoretical focus, virtually nothing is known about the mechanisms responsible for the generation of individual-level diversification. Here we report analyses of sources of variation in timing of germination within seasons, germination fraction over two generations and three sequential seasons, and the genetic correlation structure of these traits using almost 10,000 seeds from more than 100 genotypes of the monocarpic perennial Lobelia inflata. Microenvironmental analysis of time to germination suggests that extreme sensitivity to environmental gradients, or microplasticity, even within a homogeneous growth chamber, may act as an effective individual-level diversification mechanism and explains more than 30% of variance in time to germination. The heritability of within-season timing of germination was low (h 2 ϭ 0.07) but significant under homogeneous conditions. Consistent with individual-level diversification, this low h 2 was attributable not to low additive genetic variance, but to an unusually high coefficient of residual variation in time to germination. Despite high power to detect additive genetic variance in within-season diversification, it was low and indistinguishable from zero. Restricted maximum likelihood detected significant genetic variation for germination fraction (h 2 ϭ 0.18) under homogeneous conditions. Unexpectedly, this heritability was positive when measured within a generation by sibling analysis and negative when measured across generations by offspring-on-parent regression. The consistency of dormancy fraction over multiple delays, a major premise of Cohen's classic model, was supported by a strong genetic correlation (r ϭ 0.468) observed for a cohort's germination fraction over two seasons. We discuss implications of the results for the evolution of bet hedging and highlight the need for further empirical study of the causal components of diversification.Key words. Diversification bet hedging, dormancy, environmental unpredictability, heritability, microplasticity, phenotypic plasticity, seed germination. Cole's (1954) renowned result-showing that the fitness of an annual and a perennial plant are equal given that the annual produces just one seed more than the perennialprompted the development of life-history theory by underscoring the evolutionary importance of age(stage)-dependent survival. Mortality at the seed and seedling stage is expected to be much higher than at later stages, especially for annual plants that produce a large number of small seeds (Harper 1977). From the perspective of life-history evolution, the importance of the timing of germination is clear: upon germination, a plant steps from the least to the most vulnerable stage of its life cycle. Thus, the ti...

A persistent debate in evolutionary biology is one over the continuity of microevolution and macroevolution -whether macroevolutionary trends are governed by the principles of microevolution. The opposition of evolutionary trends over different time scales is taken as evidence that selection is uncoupled over these scales. I argue that the paradox inferred by trend opposition is eliminated by a hierarchical application of the Ôgeometric-mean fitnessÕ principle, a principle that has been invoked only within the limited context of microevolution in response to environmental variance. This principle implies the elimination of well adapted genotypes -even those with the highest arithmetic mean fitness over a shorter time scale. Contingent on premises concerning the temporal structure of environmental variance, selectivity of extinction, and clade-level heritability, the evolutionary outcome of major environmental change may be viewed as identical in principle to the outcome of minor environmental fluctuations over the short-term. Trend reversals are thus recognized as a fundamental property of selection operating at any phylogenetic level that occur in response to event severities of any magnitude over all time scales. This Ôbet-hedgingÕ perspective differs from others in that a specified, single hierarchical selective process is proposed to explain observed hierarchical patterns of extinction.

The presence of heritable variation in traits is a prerequisite for evolution. The great majority of heritability (h ) estimates are performed under laboratory conditions that are characterized by low levels of environmental variability. Very little is known about the effect of environmental variability on the estimation of components of quantitative variation, although theoretical extrapolations from lab studies have been attempted. Here we investigate the effects of environmental heterogeneity on variance component estimation using full-sib families of Gryllus pennsylvanicus split between a homogeneous laboratory environment and a more variable field environment. Although large standard errors prevent demonstration of statistically significant differences among h of traits measured in the two environments for all but one trait, the values of h are, on average, lower in the variable field environment, with a mean reduction of 19%. Developmental time is an exception, exhibiting high levels of additive variance in the field, leading to a higher value of h in the variable environment. Underlying the lower field h estimates are greater components of environmental variance as expected, as well as lower components of genetic variance. In this study, there is no evidence that the increase in the environmental component of variance in the field is any more important in the reduction of h than is the decrease in the additive genetic component. The implications of the relative changes in the two components of variance are discussed.