Dealing with stochastic environmental variation in space and time: bet hedging by generalist,specialist, and diversified strategies

Building on previous work, we derive an optimization model for a two-state stochastic environment and evaluate the fitnesses of five reproductive strategies across generations. To do this, we characterize spatiotemporal variation and define grain (=patch) size as the scale of fitness autocorrelation. Fitness functions of environmental condition are Gaussian. The strategies include two specialists on each of the environmental conditions; two generalists that each fare equally well under both conditions, but one (a conservative bet hedger) optimizes the shape of the fitness function; and a diversified bet hedger producing an optimal mix of the two specialists within individual broods. When the environment is primarily in one of the two states, the specialist on that state achieves the highest fitness. In the more interesting situation where the two environments are equally prevalent in the long term, with low-moderate environmental variation, a generalist strategy (that copes with both states well) does best. Higher variation favors diversified bet hedgers, or surprisingly, specialists, depending mainly on whether spatial or temporal variation predominates. These strategies reduce variance in fitness and optimize the distribution of offspring among patches differently: specialists by spreading offspring among many independently varying patches, while diversified bet hedgers put all offspring into a few patches or a single patch. We distinguish features consistent with strategies like diversified bet hedgers that spread risk in time from features linked to strategies like specialists that spread risk in space. Finally, we present testable hypotheses arising from this study and suggest directions for future work.     

Flexible dispersal strategies in native and non‐native ranges: environmental quality and the ‘good–stay,bad–disperse’ rule

Dispersal strategies are one of the most important determinants of range dynamics and a surrogate for invasiveness. We tested three inter‐related hypotheses derived from demographic and ecological models: (H₁) short‐distance dispersal strategies arise at native range margins due to their demographic advantage; (H₂) in non‐native areas a high diffusion rate is favoured at the advancing range front for niche filling; (H₃) environmental deterioration can increase dispersal and lead to a ‘good–stay, bad–disperse’ strategy. Spatially and temporally explicit rates of spread and dispersal kernels of the European starling Sturnus vulgaris were generated for its native range (Britain) using ringing records from 1909 to 2008, and for a non‐native area (South Africa) using ringing data and distributional records since its introduction in 1897. There was a marked spatial and temporal variation in the rate of spread within both native and non‐native ranges. In the native range the rate of spread declined with increasing distance from the species’ European distribution (contradicting H₁). In the non‐native range the rate of spread increased with distance from the introduction locality (supporting H₂). The annual rate of spread in the native range also increased significantly when environmental conditions were deteriorating as indicated by marked population declines and relatively low abundance (H₃), providing clear evidence for flexible dispersal strategies based on a ‘good–stay, bad–disperse’ rule. Starlings’ dispersal kernel followed an inverse power law and showed strong anisotropy and significant divergence between native and invasive populations, suggesting a flexible strategy comprising a dynamic response to spatial and temporal environmental variation with implications for predicting dispersal and range dynamics arising from environmental change.     

Evolution of dispersal in a multi‐trophic community context

Much is known about the evolution of dispersal when species interact with their resources or natural enemies, but very little is known about dispersal evolution when species interact with both resources and natural enemies. Here I investigate how the dispersal of an intermediate consumer evolves in response to its interactions with a basal resource and top predator. I find that dispersal evolution is possible even when the consumer species is not directly affected by environmental variability, but rather experiences the consequences that such variability has on its resource and predator. Spatial variation in the consumer's fitness is driven by spatial heterogeneity in resource productivity, which determines whether a predator can colonize a resource‐consumer community. Temporal variation in the consumer's fitness is driven by random disturbances that cause periodic local extinctions of the predator, followed by recolonizations that lead to transient fluctuations in consumer abundance. When spatial variation in resource productivity is low and the predator can colonize all patches in the landscape, there is no spatial variation in consumer fitness but temporal variation in fitness favors the evolution of a dispersal monomorphism. When spatial variation in resource productivity is high and the predator cannot colonize many patches in the landscape, spatial variation in fitness selects against dispersal. In this case, temporal variation can promote the evolution of a dispersal polymorphism with sedentary and mobile phenotypes, but only for certain types of tri‐trophic interactions. This finding underscores the importance of indirect interactions in shaping the evolution of dispersal. While the ecological community can provide a strong selective environment for the evolution of dispersal, the nature of interactions between trophic levels can also impose constraints on evolution.     

Microhabitat heterogeneity influences offspring sex allocation and spatial kin structure in possums

1. Sex allocation theory predicts that where dispersal is sex biased, the fitness consequences of producing male or female offspring are mediated by resource availability and maternal competitive ability. Females in poorer condition are expected to favour dispersing offspring to minimize resource competition with kin. Environmental heterogeneity may drive spatial variation in sex allocation through resource competition-related benefits to females and territory quality benefits to dispersing or philopatric offspring. 2. Here, we demonstrate that microhabitat heterogeneity can drive extremely fine-scale spatial heterogeneity in offspring sex allocation. Female bobucks (Trichosurus cunninghami) in temperate rainforest were more likely to produce male offspring than those in surrounding Eucalyptus forest. 3. A maternal physiological effect was identified, in that females of lower body mass were more likely to produce male offspring. This finding is consistent with resource competition predictions, in that smaller females are expected to have poorer competitive ability. 4. Genetic spatial autocorrelation analysis identified males as the more dispersing sex. Furthermore, overproduction of males by mothers in the rainforest habitat was geographically concordant with reduced philopatry, as inferred from spatial genetic analysis. This provides empirical validation of dispersal-related explanations of offspring sex allocation: that production of offspring of the dispersing sex minimizes the potential for resource competition with kin. 5. Spatial variation in dispersal via sex allocation responses to environmental heterogeneity can potentially contribute to spatial patterns in population dynamics.     

The population-dynamic functions of seed dispersal

We summarize some of the population-dynamic consequences of the mosaic structure of plant populations for the evolution of seed dispersal. A fairly elaborated set of theoretical ideas exist regarding the evolution of dispersal and we have synthesized some of them in an attempt to make them more accessible to field ecologists. We consider the relationship of these general theoretical ideas to our understanding of fruit and seed dispersal.We develop three related models to describe the similarities and differences in how dispersal functions for risk reduction (bet hedging), escaping the negative consequences of crowding, and escaping high concentrations of relatives. We also briefly discuss directed dispersal as a fourth population-dynamic aspect of dispersal. Dispersal can have a risk-reducing function only when there is global (metapopulation) temporal variance in success. Dispersal to escape the negative consequences of crowding requires only spatial and local temporal environmental variation. Dispersal for escaping high concentrations of relatives requires no environmental variation, but does require genetic population structure. Directed dispersal, defined as non-random into particular patch types contingent on the expectation of local success, is always valuable when possible and represents an advantage independent the others which can occur with random dispersal.In an effort to accommodate for the differences between simple mathematical models and the behavior of complex natural fruit and seed dispersal systems we have discussed the following issues: actual patterns of patch structure and dispersal distance; the implications of plant cosexuality, perenniality, and allocation costs of dispersal structures; and the impact of the detailed nature of density dependence, breeding systems, and genetic structure. We briefly compare the population-dynamic functions of dispersal presented here with the widely cited functions of colonization, escape, and directed dispersal. Finally, we suggest how the theoretical models can be used with field data to estimate the fitness consequences of dispersal.     

FINE-GRAINED SPATIAL AND TEMPORAL VARIATION IN SELECTION DOES NOT MAINTAIN GENETIC VARIATION IN ERIGERON ANNUUS

Because interactions among plants are spatially local, the scale of environmental heterogeneity can have large effects on evolutionary dynamics. However, very little is known about the spatial patterns of variation in fitness and the relative magnitude of spatial and temporal variation in selection. Replicates of 12 genotypes of Erigeron annuus (Asteraceae) were planted in 288 locations within a field, separated by distances of 0.1 to 30.0 m, and replicated in two years. In a given year, most spatial variation in relative fitness (genotype-environment [G × E] interactions for fitness) occurred over distances of only 50 cm. Year effects were as large or larger than the spatial variation in fitness; in particular there was a large, three-way, genotype-year-environment interaction at the smallest spatial scale. The genetic correlation of fitness across years at a given location was near zero, 0.03. Thus, the relative fitness of genotypes is spatially unpredictable and a map of the selective environment has constantly shifting locations of peaks and valleys. Including measurements of soil nutrients as covariates in the analysis removed most of the spatial G × E interaction. Vegetation and microtopography had no effect on the G × E terms, suggesting that differential response to soil nutrients is the cause of spatial variation in fitness. However, the slope of response to NH₄ and P0₄ was negative; therefore the soil nutrients are probably just indicators of other, unknown, environmental factors. We explored via simulation the evolutionary consequences of spatial and temporal variation in fitness and showed that, for this system, the spatial scale of variation was too fine grained (by a factor of 3 to 5) to be a powerful force maintaining genetic variation in the population. The inclusion of both spatial and temporal variation in fitness actually reduced the coexistence of genotypes compared to pure spatial models. Thus the presence of spatial or temporal variation in selection does not guarantee that it is an effective evolutionary force maintaining diversity. Instead the pattern of selection favors generalist genotypes.     

Linking the spatial scale of environmental variation and the evolution of phenotypic plasticity: selection favors adaptive plasticity in fine-grained environments

Adaptive phenotypic plasticity and adaptive genetic differentiation enable plant lineages to maximize their fitness in response to environmental heterogeneity. The spatial scale of environmental variation relative to the average dispersal distance of a species determines whether selection will favor plasticity, local adaptation, or an intermediate strategy. Habitats where the spatial scale of environmental variation is less than the dispersal distance of a species are fine grained and should favor the expression of adaptive plasticity, while coarse-grained habitats, where environmental variation occurs on spatial scales greater than dispersal, should favor adaptive genetic differentiation. However, there is relatively little information available characterizing the link between the spatial scale of environmental variation and patterns of selection on plasticity measured in the field. I examined patterns of spatial environmental variation within a serpentine mosaic grassland and selection on an annual plant (Erodium cicutarium) within that landscape. Results indicate that serpentine soil patches are a significantly finer-grained habitat than non-serpentine patches. Additionally, selection generally favored increased plasticity on serpentine soils and diminished plasticity on non-serpentine soils. This is the first empirical example of differential selection for phenotypic plasticity in the field as a result of strong differences in the grain of environmental heterogeneity within habitats.     

Interactions between spatial and temporal scales in the evolution of dispersal rate

The evolution of dispersal rate is studied with a model of several local populations linked by dispersal. Three dispersal strategies are considered where all, half or none of the offspring disperse. The spatial scale (number of patches) and the temporal scale (probability of local extinction) of the environment are critical in determining the selective advantage of the different dispersal strategies. The results from the simulations suggest that an interaction between group selection and individual selection results in a different outcome in relation to the spatial and temporal scales of the environment. Such an interaction is able to maintain a polymorphism in dispersal strategies. The maintenance of this polymorphism is also scale-dependent. This study suggests a mechanism for the short-term evolution of dispersal, and provides a testable prediction of this hypothesis, namely that loss of dispersal abilities should be more frequent in spatially more continuous environments, or in temporally more stable environments. This revised version was published online in July 2006 with corrections to the Cover Date.     

The effect of female polyandry and sperm precedence on the evolution of sexual difference in dispersal timing

Predispersal copulation and unpredictable environment facilitate the evolution of female-biased dispersal in species, where females are functionally monandrous. Females should migrate and reproduce over different habitats to spread their risks due to environmental fluctuation. On the other hand, males do not have to disperse because their risks are spread by their mating partners who produce their offspring in different habitats. However, when females are functionally polyandrous, it is expected that they will not contribute to spreading the male's risk extensively. Therefore, by simulation with the individual based model, the present study evaluated how female polyandry influences the sexual difference in dispersal timing. This model revealed that when females are polyandrous, the timing of female remating and sperm priority patterns have an important influence on the evolution of sex-biased dispersal. Particularly when female remating is not synchronized with dispersal or when last-male sperm precedence does not exist, female-biased dispersal is evolved.     

Size and survival in a stochastic environment

Summary Spatial and temporal variability in environmental conditions can significantly influence fluctuations in body size if the environmental heterogeneity gives rise to variable size dependent mortality rates, or dispersal between sites incurs a reproductive cost. Temporal variability has a greater effect than spatial variability. These conclusions are derived from a model based on the assumption that the innate capacity for increase, r _m , is a suitable fitness measure. The limitations of this model are discussed and an alternative approach using the parent-offspring regression presented. It is suggested that models based upon the latter approach are more appropriate for investigations of the evolution of traits (showing continuous variation) in variable environments because it does not require the assumption that some fitness measure is being optimized and because it may give more insight into the rates of change of the character.     

Population differentiation in an annual legume: local adaptation

Abstract. Studies of many plants species have demonstrated adaptive genetic differentiation to local environmental conditions. Typically these studies are conducted to evaluate adaptation to contrasting environments. As a consequence, although local adaptation has been frequently demonstrated, we have little information as to the spatial scale of adaptive evolution. We evaluated adaptive differentiation between populations of the annual legume Chamaecrista fasciculata using a replicated common-garden design. Study sites were established in three field locations that are home to native populations of C. fasciculata . Each location was planted for two years with seed from the population native to the study site (home population) and populations located six distances (0.1-2000 km) from each site (transplanted populations). Seeds were planted into the study sites with minimum disturbance to determine the scale of local adaptation, as measured by a home-site fitness advantage, for five fitness components: germination, survival, vegetative biomass, fruit production, and the number of fruit produced per seed planted (an estimate of cumulative fitness). For all characters there was little evidence for local adaptation, except at the furthest spatial scales. Patterns of adaptive differentiation were fairly consistent in two of the three sites, but varied between years. Little genetic variation was expressed at the third site. These results, combined with previous estimates of limited gene flow, suggest that metapopulation processes and temporal environmental variation act together to reduce local adaptation, except over long distances.     

The cost of reproduction induced by body size at birth and breeding density

Body size at birth has implications for the quality of individuals throughout their life. Although large body size is generally considered an advantage, the relationship between body size at birth and long-term fitness is often complicated. Under spatial or temporal variation in environmental conditions, such as the seasonally changing densities of Fennoscandian vole populations, selection should favor variation in offspring phenotypes, as different qualities may be beneficial in different conditions. We performed an experiment in which a novel hormonal manipulation method was used to increase phenotypic variance in body size at birth in the bank vole (Myodes glareolus). The effects of body size on the future fitness of young males and females were then studied at varying population densities in outdoor enclosures. Our results show that small body size at birth and high breeding density increase the survival costs of reproduction. However, there was no interaction between the effects of body size and density on survival, which suggests that the fitness effects of body size were strong enough to persist under environmental variation. Moreover, litter size and the probability of breeding were more sensitive to variation in breeding density than offspring size. Therefore, it is unlikely that individual fitness could be optimized by adjusting offspring body size to the prevailing population density through adaptive maternal effects. Our results highlight the significance of the costs of reproduction in the evolution of life-history traits, and give strong experimental support for the long-term fitness effects of body size at birth.     

GENOTYPE-BY-ENVIRONMENT INTERACTIONS FOR FITNESS OF ERIGERON ANNUUS SHOW FINE-SCALE SELECTIVE HETEROGENEITY

The results of natural selection depend critically on whether variation in fitness is finegrained or coarse-grained with respect to dispersal, but little is known of the spatial scale of fitness variation in natural populations. For most evolutionary questions, environmental heterogeneity must be defined by reversals in the relative fitness of genotypes; absolute fitness may vary, but if genotypes respond in parallel then selection is uniform. Thus, measurements of genotype-by-environment (G × E) interactions for fitness are necessary to understand patterns of variation in natural selection.     

Metacommunity Structure of Stream Insects across Three Hierarchical Spatial scales

A major challenge in community ecology is to understand the underlying factors driving metacommunity (i.e., a set of local communities connected through species dispersal) dynamics. However, little is known about the effects of varying spatial scale on the relative importance of environmental and spatial (i.e., dispersal related) factors in shaping metacommunities and on the relevance of different dispersal pathways. Using a hierarchy of insect metacommunities at three spatial scales (a small, within‐stream scale, intermediate, among‐stream scale, and large, among‐sub‐basin scale), we assessed whether the relative importance of environmental and spatial factors shaping metacommunity structure varies predictably across spatial scales, and tested how the importance of different dispersal routes vary across spatial scales. We also studied if different dispersal ability groups differ in the balance between environmental and spatial control. Variation partitioning showed that environmental factors relative to spatial factors were more important for community composition at the within‐stream scale. In contrast, spatial factors (i.e., eigenvectors from Moran's eigenvector maps) relative to environmental factors were more important at the among‐sub‐basin scale. These results indicate that environmental filtering is likely to be more important at the smallest scale with highest connectivity, while dispersal limitation seems to be more important at the largest scale with lowest connectivity. Community variation at the among‐stream and among‐sub‐basin scales were strongly explained by geographical and topographical distances, indicating that overland pathways might be the main dispersal route at the larger scales among more isolated sites. The relative effect of environmental and spatial factors on insect communities varied between low and high dispersal ability groups; this variation was inconsistent among three hierarchical scales. In sum, our study indicates that spatial scale, connectivity, and dispersal ability jointly shape stream metacommunities.     

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

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

Spatial heterogeneity and rates of spread in experimental streams

Theoretical models predict that environmental heterogeneity can decrease or potentially increase rates of spread in biological populations depending on the relationship between the scale of dispersal and the scale of heterogeneity. These effects arise from the interaction between habitat quality and the processes of dispersal, colonization and growth. Flowing water environments provide a unique opportunity to test these predictions. If advection influences dispersal, flow can alter the relative scale of dispersal to environmental heterogeneity in the upstream versus downstream direction. We explored the influence of heterogeneity on the spatial spread of a species of diatom in experimental streams. Environmental heterogeneity was created by maintaining agar diffusing substrata at different nutrient levels. Diatoms were placed at the midpoint of each stream, and spatial spread rates were determined by monitoring algal abundance non‐destructively. Our results reveal that, relative to homogeneous streams, resource heterogeneity decreases spread rate in the upstream direction but increases spread rate in the downstream direction. Empirical estimates of growth rates and colonization times reveal that heterogeneity predominantly influenced colonization rates. Colonization rates estimate successful dispersal events, and thus relate to both colonization and dispersal. These results are one of the first empirical tests of general theories regarding the impact of heterogeneity on rates of spread and highlight the importance of understanding the impact of heterogeneity on colonization and dispersal in continuous habitats.     

Establishment versus population growth in spatio-temporally varying environments

We consider situations where repeated invasion attempts occur from a source population into a receptor population over extended periods of time. The receptor population contains two locations that provide different expected offspring numbers to invaders. There is demographic stochasticity in offspring numbers. In addition, temporal variation causes local invader fitnesses to vary. We show that effects of environmental autocorrelation on establishment success depend on spatial covariance of the receptor subpopulations. In situations with a low spatial covariance this effect is positive, whereas high spatial covariance and/or high migration probabilities between the subpopulations causes the effect to be negative. This result reconciles seemingly contradictory results from the literature concerning effects of temporal variation on population dynamics with demographic stochasticity. We study an example in the context of genetic introgression, where invasions of cultivar plant genes occur through pollen flow from a source population into wild-type receptor populations, but our results have implications in a wider range of contexts, such as the spread of exotic species, metapopulation dynamics and epidemics.     

WHAT DETERMINES FITNESS WHEN DISPERSAL IS LIMITED?

Simple evolutionary models typically assume a homogeneous environment in which all individuals have equal access to resources. However, when dispersal is limited this assumption is unlikely to correspond to reality. Instead, the offspring of relatively fecund parents can be expected to find that resources are scarce because of competition from their relatively large number of siblings. We show that these factors lead to selection for decreased variation in the number of offspring produced. We investigate the relationship between fitness and variation in fertility for a variety of different circumstances. Our results indicate that, in some cases, selection for reduced variation in fertility can be very substantial.     

Inside‐container effects drive mosquito community structure in Brazilian Atlantic forest

Metacommunity theory is a convenient framework in which to investigate how local communities linked by dispersal influence patterns of species distribution and abundance across large spatial scales. For organisms with complex life cycles, such as mosquitoes, different pressures are expected to act on communities due to behavioral and ecological partitioning of life stages. Adult females select habitats for oviposition, and resulting offspring are confined to that habitat until reaching adult stages capable of flight; outside‐container effects (OCE) (i.e., spatial factors) are thus expected to act more strongly on species distributions as a function of adult dispersal capability, which should be limited by geographic distances between sites. However, larval community dynamics within a habitat are influenced by inside‐container effects (ICE), mainly interactions with conspecifics and heterospecifics (e.g., through effects of competition and predation). We used a field experiment in a mainland‐island scenario to assess whether environmental, spatial, and temporal factors influence mosquito prey and predator distributions and abundances across spatial scales: within‐site, between‐site, and mainland‐island. We also evaluated whether predator abundances inside containers play a stronger role in shaping mosquito prey community structure than do OCE (e.g., spatial and environmental factors). Temporal influence was more important for predators than for prey mosquito community structure, and the changes in prey mosquito species composition over time appear to be driven by changes in predator abundances. There was a negligible effect of spatial and environmental factors on mosquito community structure, and temporal effects on mosquito abundances and distributions appear to be driven by changes in abundance of the dominant predator, perhaps because ICE are stronger than OCE due to larval habitat restriction, or because adult dispersal is not limited at the chosen spatial scales.     

Selection for increased allocation to offspring number under environmental unpredictability

According to life-history theory, the evolution of offspring size is constrained by the trade-off between allocation of resources to individual offspring and the number of offspring produced. Existing models explore the ecological consequences of offspring size, whereas number is invariably treated simply as an outcome of the trade-off with size. Here I ask whether there is a direct evolutionary advantage of increased allocation to offspring number under environmental unpredictability. Variable environments are expected to select for diversification in the timing of egg hatch and seed germination, yet the dependence of the expression of diversification strategies, and thus parental fitness, on offspring number has not previously been recognized. I begin by showing that well-established sampling theory predicts that a target bethedging diversification strategy is more reliably achieved as offspring number increases. I then use a simulation model to demonstrate that higher offspring number leads to greater geometric mean fitness under environmental uncertainty. Natural selection is thus expected to act directly to increase offspring number under assumptions of environmental unpredictability in season quality.