Adaptive Transgenerational Plasticity Research Articles

Transgenerational plasticity in aphids reared in a poor-resource environment

The changing environmental conditions can affect insect biology over multiple generations and phenotypic plasticity is important for coping with these changes. Transgenerational plasticity occurs when the environment in which the parents developed influences the plastic response of the offspring phenotype. In the present study, the plastic effects of resource limitation on important life history traits such as body size, fecundity, survival, and resistance to starvation of the pea aphid Acyrthosiphon pisum were investigated over two generations. This study focused on understanding how resource limitation can determine an adaptive expression of maternal effects and transgenerational plasticity in fitness-related traits. Aphids showed phenotypic plasticity for the life history traits investigated, as they performed better when grown in an optimal environment than in a resource-poor one. Also, aphids had a poorer performance if their mothers were raised in a resource-poor environment. The effects of transgenerational plasticity were observed only in response to resistance to starvation, through increased survival in the offspring of the mother reared in a resource-poor environment, suggesting an evolutionary bet-hedging strategy. The results of this study showed that the effects of adaptive transgenerational plasticity may be partially masked in stressful environments, where developmental problems instead predominate. More information on the transgenerational response to resource limitation across generations can contribute to a better understanding of aphid biology.

Heat stress reveals a fertility debt owing to postcopulatory sexual selection.

Climates are changing rapidly, demanding equally rapid adaptation of natural populations. Whether sexual selection can aid such adaptation is under debate; while sexual selection should promote adaptation when individuals with high mating success are also best adapted to their local surroundings, the expression of sexually selected traits can incur costs. Here we asked what the demographic consequences of such costs may be once climates change to become harsher and the strength of natural selection increases. We first adopted a classic life history theory framework, incorporating a trade-off between reproduction and maintenance, and applied it to the male germline to generate formalized predictions for how an evolutionary history of strong postcopulatory sexual selection (sperm competition) may affect male fertility under acute adult heat stress. We then tested these predictions by assessing the thermal sensitivity of fertility (TSF) in replicated lineages of seed beetles maintained for 68 generations under three alternative mating regimes manipulating the opportunity for sexual and natural selection. In line with the theoretical predictions, we find that males evolving under strong sexual selection suffer from increased TSF. Interestingly, females from the regime under strong sexual selection, who experienced relaxed selection on their own reproductive effort, had high fertility in benign settings but suffered increased TSF, like their brothers. This implies that female fertility and TSF evolved through genetic correlation with reproductive traits sexually selected in males. Paternal but not maternal heat stress reduced offspring fertility with no evidence for adaptive transgenerational plasticity among heat-exposed offspring, indicating that the observed effects may compound over generations. Our results suggest that trade-offs between fertility and traits increasing success in postcopulatory sexual selection can be revealed in harsh environments. This can put polyandrous species under immediate risk during extreme heat waves expected under future climate change.

Exploring links between climatic predictability and the evolution of within‐ and transgenerational plasticity

In variable environments, phenotypic plasticity can increase fitness by providing tight environment-phenotype matching. However, adaptive plasticity is expected to evolve only when the future selective environment can be predicted based on the prevailing conditions. That is, the juvenile environment should be predictive of the adult environment (within-generation plasticity) or the parental environment should be predictive of the offspring environment (transgenerational plasticity). Moreover, the environmental predictability can also shape transient responses such as stress response in an adaptive direction. Here, we test links between environmental predictability and the evolution of adaptive plasticity by combining time series analyses and a common garden experiment using temperature as a stressor in a temperate butterfly (Melitaea cinxia). Time series analyses revealed that across season fluctuations in temperature over 48 years are overall predictable. However, within the growing season, temperature fluctuations showed high heterogeneity across years with low autocorrelations and the timing of temperature peaks were asynchronous. Most life-history traits showed strong within-generation plasticity for temperature and traits such as body size and growth rate broke the temperature-size rule. Evidence for transgenerational plasticity, however, was weak and detected for only two traits each in an adaptive and non-adaptive direction. We suggest that the low predictability of temperature fluctuations within the growing season likely disfavors the evolution of adaptive transgenerational plasticity but instead favors strong within-generation plasticity.

Local adaptation in the transgenerational response to copper pollution in the bryozoan Bugula neritina.

Transgenerational plasticity (TGP)-when a parent or previous generation's environmental experience affects offspring phenotype without involving a genetic change-can be an important mechanism allowing for rapid adaptation. However, despite increasing numbers of empirical examples of TGP, there appears to be considerable variation in its strength and direction, yet limited understanding of what causes this variation. We compared patterns of TGP in response to stress across two populations with high versus low historical levels of stress exposure. Specifically, we expected that exposure to acute stress in the population experiencing historically high levels of stress would result in adaptive TGP or alternatively fixed tolerance (no parental effect), whereas the population with low levels of historical exposure would result in negative parental carryover effects. Using a common sessile marine invertebrate, Bugula neritina, and a split brood design, we exposed parents from both populations to copper or control treatments in the laboratory and then had them brood copper-naïve larvae. We then exposed half of each larval brood to copper and half to control conditions before allowing them to grow to maturity in the field. Maternal copper exposure had a strong negative carryover effect on adult offspring growth and survival in the population without historical exposure, especially when larvae themselves were exposed to copper. We found little to no maternal or offspring treatment effect on adult growth and survival in the population with a history of copper exposure. However, parents from this population produced larger larvae on average and were able to increase the size of their larvae in response to copper exposure, providing a potential mechanism for maintaining fitness and suggesting TGP through maternal provisioning. These results indicate that the ability to adjust offspring phenotype via TGP may be a locally adapted trait and potentially influenced by past patterns of exposure.

Transgenerational non-genetic inheritance has fitness costs and benefits under recurring stress in the clonal duckweed Spirodela polyrhiza.

Although non-genetic inheritance is thought to play an important role in plant ecology and evolution, evidence for adaptive transgenerational plasticity is scarce. Here, we investigated the consequences of copper excess on offspring defences and fitness under recurring stress in the duckweed Spirodela polyrhiza across multiple asexual generations. Growing large monoclonal populations (greater than 10 000 individuals) for 30 generations under copper excess had negative fitness effects after short and no fitness effect after prolonged growth under recurring stress. These time-dependent growth rates were likely influenced by environment-induced transgenerational responses, as propagating plants as single descendants for 2 to 10 generations under copper excess had positive, negative or neutral effects on offspring fitness depending on the interval between initial and recurring stress (5 to 15 generations). Fitness benefits under recurring stress were independent of flavonoid accumulations, which in turn were associated with altered plant copper concentrations. Copper excess modified offspring fitness under recurring stress in a genotype-specific manner, and increasing the interval between initial and recurring stress reversed these genotype-specific fitness effects. Taken together, these data demonstrate time- and genotype-dependent adaptive and non-adaptive transgenerational responses under recurring stress, which suggests that non-genetic inheritance alters the evolutionary trajectory of clonal plant lineages in fluctuating environments.

Empirical patterns of environmental variation favor adaptive transgenerational plasticity.

Effects of parental environment on offspring traits have been well known for decades. Interest in this transgenerational form of phenotypic plasticity has recently surged due to advances in our understanding of its mechanistic basis. Theoretical research has simultaneously advanced by predicting the environmental conditions that should favor the adaptive evolution of transgenerational plasticity. Yet whether such conditions actually exist in nature remains largely unexplored. Here, using long‐term climate data, we modeled optimal levels of transgenerational plasticity for an organism with a one‐year life cycle at a spatial resolution of 4 km2 across the continental United States. Both annual temperature and precipitation levels were often autocorrelated, but the strength and direction of these autocorrelations varied considerably even among nearby sites. When present, such environmental autocorrelations render offspring environments statistically predictable based on the parental environment, a key condition for the adaptive evolution of transgenerational plasticity. Results of our optimality models were consistent with this prediction: High levels of transgenerational plasticity were favored at sites with strong environmental autocorrelations, and little‐to‐no transgenerational plasticity was favored at sites with weak or nonexistent autocorrelations. These results are among the first to show that natural patterns of environmental variation favor the evolution of adaptive transgenerational plasticity. Furthermore, these findings suggest that transgenerational plasticity is likely variable in nature, depending on site‐specific patterns of environmental variation.

Seed Germination Indicates Adaptive Transgenerational Plasticity in a Submerged Macrophyte.

Adaptive transgenerational plasticity is an important evolutionary strategy in plants. We investigated the resource allocation strategy in sexual reproduction and performed an in situ seed germination experiment of Potamogeton maackianus to reveal their responses to different water depths. Later, we discussed the biased adaptability to the maternal habitat in this species. We found a positive correlation between sexual and asexual reproduction in water depths from 1.0 m to 3.0 m, such a correlation failed to occur in 4.0 m water depth. These results indicate that the trade-off between sexual and asexual reproduction should only be expected in a stressful habitat, where resource acquisition is limited. For trade-off between quantity and quality of sexual units in different water depths, P. maackianus tends to produce more but lower quality sexual reproductive units in shallow water, and fewer but higher quality sexual units are found in deep water. The total germination percentage of seeds of P. maackianus was relatively poor, less than 46.65% in all of the treatments. The maximum germination percentage of seeds from 1.0 m, 2.0 m, 3.0 m, and 4.0 m water depths are 14.4%, 17.75%, 25.51%, and 46.65%, respectively. Seeds with higher germination percentage were from deeper water depths. The most interesting result was that the maximum final germination percentage occurred only when treatment water depth was the same as collection water depth. Our result showed that the variations in germination characters of the studied species appear to be based partly on the effects of maternal environmental factors. Our findings proved the adaptive transgenerational plasticity in P. maackianus, which will play an important role in evolutionary response to the selection of water depths.

The evolution of epigenetically mediated adaptive transgenerational plasticity in a subdivided population.

Transgenerational plasticity (TGP) occurs when offspring exhibit plasticity in traits induced by the environments experienced by their parents, and represents a nongenetic mechanism of inheritance. Evidence that traits can be transmitted to future generations by means other than genetic inheritance has caused a surge of interest in epigenetic inheritance, but evidence for epigenetic modifications being both adaptive and heritable remains scarce. What features would make a species most prone to evolve a system of epigenetically mediated adaptive TGP? Here, we use population-genetic models modified to include epigenetic induction and inheritance to investigate if and when epigenetically mediated adaptive TGP would be expected to evolve for a population subdivided between two habitats connected by migration. We show that differences in the direction of selection between the two habitats drives the evolution of epigenetically mediated adaptive TGP. With low migration, the strength of indirect selection in favor of epigenetically mediated adaptive TGP increases with migration rate. Yet, with higher migration, the opposite trend is observed. We predict that species subdivided between habitats that differ in the direction of selection with moderate migration rates between the habitats would be most likely to evolve epigenetically mediated adaptive TGP if costs of producing such systems are not too high.

Transgenerational plasticity and selection shape the adaptive potential of sticklebacks to salinity change.

In marine climate change research, salinity shifts have been widely overlooked. While widespread desalination effects are expected in higher latitudes, salinity is predicted to increase closer to the equator. We took advantage of the steep salinity gradient of the Baltic Sea as a space‐for‐time design to address effects of salinity change on populations. Additionally, genetic diversity, a prerequisite for adaptive responses, is reduced in Baltic compared to Atlantic populations. On the one hand, adaptive transgenerational plasticity (TGP) might buffer the effects of environmental change, which may be of particular importance under reduced genetic variation. On the other hand, physiological trade‐offs due to environmental stress may hamper parental provisioning to offspring thereby intensifying the impact of climate change across generations (nonadaptive TGP). Here, we studied both hypothesis of adaptive and nonadaptive TGP in the three‐spined stickleback (Gasterosteus aculeatus) fish model along the strong salinity gradient of the Baltic Sea in a space‐for‐time experiment. Each population tolerated desalination well, which was not altered by parental exposure to low salinity. Despite a common marine ancestor, populations locally adapted to low salinity lost their ability to cope with fully marine conditions, resulting in lower survival and reduced relative fitness. Negative transgenerational effects were evident in early life stages, but disappeared after selection via mortality occurred during the first 12–30 days posthatch. Modeling various strengths of selection, we showed that nonadaptive transgenerational plasticity accelerated evolution by increasing directional selection within the offspring generation. Qualitatively, when genetic diversity is large, we predict that such effects will facilitate rapid adaptation and population persistence, while below a certain threshold populations suffer a higher risk of local extinction. Overall, our results suggest that transgenerational plasticity and selection are not independent of each other and thereby highlight a current gap in TGP studies.

Transgenerational plasticity in Silene vulgaris in response to three types of stress.

The environment experienced by plants can influence the phenotype of their offspring. Such transgenerational plasticity can be adaptive when it results in higher fitness of the offspring under conditions correlated with those experienced by the mother plant. However, it has rarely been tested if such anticipatory parental effects may be induced with different environments. We grew clonal replicates of Silene vulgaris under control conditions and three types of stress (nutrient deficiency, copper addition and drought), which are known from natural populations of the species. We then subjected offspring from differently treated mother plants to each of the different stress treatments to analyse the influence of maternal and offspring environment on performance and several functional traits. Current stress treatments strongly influenced biomass and functional traits of the plants, mostly in line with responses predicted by the theory of functional equilibrium. Plant performance was also influenced by maternal stress treatments, and some effects independent of initial size differences remained until harvest. In particular, stressed mothers produced offspring of higher fitness than control plants. However, there was no evidence for treatment-specific adaptive transgenerational plasticity, as offspring from a mother plant that had grown in a specific environment did not grow better in that environment than other plants. Our results indicate that the maternal environment may affect offspring traits and performance, but also that this transgenerational plasticity is not necessarily adaptive.

Transgenerational stress-adaption: an opportunity for ecological epigenetics.

In the recent years, there has been considerable interest to investigate the adaptive transgenerational plasticity of plants and how a "stress memory" can be transmitted to the following generation. Although, increasing evidence suggests that transgenerational adaptive responses have widespread ecological relevance, the underlying epigenetic processes have rarely been elucidated. On the other hand, model plant species have been deeply investigated in their genome-wide methylation landscape without connecting this to the ecological reality of the plant. What we need is the combination of an ecological understanding which plant species would benefit from transgenerational epigenetic stress-adaption in their natural habitat, combined with a deeper molecular analysis of non-model organisms. Only such interdisciplinary linkage in an ecological epigenetic study could unravel the full potential that epigenetics could play for the transgenerational stress-adaption of plants.

Trans-generational plasticity in response to immune challenge is constrained by heat stress.

Trans‐generational plasticity (TGP) is the adjustment of phenotypes to changing habitat conditions that persist longer than the individual lifetime. Fitness benefits (adaptive TGP) are expected upon matching parent–offspring environments. In a global change scenario, several performance‐related environmental factors are changing simultaneously. This lowers the predictability of offspring environmental conditions, potentially hampering the benefits of TGP. For the first time, we here explore how the combination of an abiotic and a biotic environmental factor in the parental generation plays out as trans‐generational effect in the offspring. We fully reciprocally exposed the parental generation of the pipefish Syngnathus typhle to an immune challenge and elevated temperatures simulating a naturally occurring heatwave. Upon mating and male pregnancy, offspring were kept in ambient or elevated temperature regimes combined with a heat‐killed bacterial epitope treatment. Differential gene expression (immune genes and DNA‐ and histone‐modification genes) suggests that the combined change of an abiotic and a biotic factor in the parental generation had interactive effects on offspring performance, the temperature effect dominated over the immune challenge impact. The benefits of certain parental environmental conditions on offspring performance did not sum up when abiotic and biotic factors were changed simultaneously supporting that available resources that can be allocated to phenotypic trans‐generational effects are limited. Temperature is the master regulator of trans‐generational phenotypic plasticity, which potentially implies a conflict in the allocation of resources towards several environmental factors. This asks for a reassessment of TGP as a short‐term option to buffer environmental variation in the light of climate change.

Evolutionary “Bet-Hedgers” under Cultivation: Investigating the Domestication of Erect Knotweed (Polygonum erectum L.) using Growth Experiments

Evolutionary “bet-hedging” refers to situations in which organisms sacrifice mean fitness for a reduction in fitness variance over time. Germination heteromorphism is the quintessential and most well understood bet-hedging strategy. It has evolved in many different plants, including the wild progenitors of some crops. Erect knotweed (Polygonum erectum L.), an annual seed crop, was cultivated in Eastern North America between c. 3000–600 BP. By c. 900 BP, cultivation had produced a domesticated subspecies with greatly reduced germination heteromorphism. Field observations and greenhouse experiments suggest that cultivation eliminated the selective pressures that maintain the bet-hedging strategy in erect knotweed, while humans also directly selected for seeds that germinated reliably and for seedlings with rapid early growth. The protection provided to erect knotweed under cultivation explains the domestication syndrome that has been observed in some archaeological assemblages. Dormancy provides seeds a means of escaping adverse conditions in time, while dispersal provides an escape in space. Farmers relaxed selective pressures that maintained dormancy in erect knotweed by acting as seed dispersers, spreading disturbance-adapted plants to predictable and protected environments, and by saving and exchanging seed stock. Experimental data also indicate that adaptive transgenerational plasticity may have been working against the expression of domestication syndrome in this case.

DNA methylation mediates genetic variation for adaptive transgenerational plasticity.

Environmental stresses experienced by individual parents can influence offspring phenotypes in ways that enhance survival under similar conditions. Although such adaptive transgenerational plasticity is well documented, its transmission mechanisms are generally unknown. One possible mechanism is environmentally induced DNA methylation changes. We tested this hypothesis in the annual plant Polygonum persicaria, a species known to express adaptive transgenerational plasticity in response to parental drought stress. Replicate plants of 12 genetic lines (sampled from natural populations) were grown in dry versus moist soil. Their offspring were exposed to the demethylating agent zebularine or to control conditions during germination and then grown in dry soil. Under control germination conditions, the offspring of drought-stressed parents grew longer root systems and attained greater biomass compared with offspring of well-watered parents of the same genetic lines. Demethylation removed these adaptive developmental effects of parental drought, but did not significantly alter phenotypic expression in offspring of well-watered parents. The effect of demethylation on the expression of the parental drought effect varied among genetic lines. Differential seed provisioning did not contribute to the effect of parental drought on offspring phenotypes. These results demonstrate that DNA methylation can mediate adaptive, genotype-specific effects of parental stress on offspring phenotypes.

Transgenerational plasticity following a dual pathogen and stress challenge in fruit flies.

BackgroundPhenotypic plasticity operates across generations, when the parental environment affects phenotypic expression in the offspring. Recent studies in invertebrates have reported transgenerational plasticity in phenotypic responses of offspring when the mothers had been previously exposed to either live or heat-killed pathogens. Understanding whether this plasticity is adaptive requires a factorial design in which both mothers and their offspring are subjected to either the pathogen challenge or a control, in experimentally matched and mismatched combinations. Most prior studies exploring the capacity for pathogen-mediated transgenerational plasticity have, however, failed to adopt such a design. Furthermore, it is currently poorly understood whether the magnitude or direction of pathogen-mediated transgenerational responses will be sensitive to environmental heterogeneity. Here, we explored the transgenerational consequences of a dual pathogen and stress challenge administered in the maternal generation in the fruit fly, Drosophila melanogaster. Prospective mothers were assigned to a non-infectious pathogen treatment consisting of an injection with heat-killed bacteria or a procedural control, and a stress treatment consisting of sleep deprivation or control. Their daughters and sons were similarly assigned to the same pathogen treatment, prior to measurement of their reproductive success.ResultsWe observed transgenerational interactions involving pathogen treatments of mothers and their offspring, on the reproductive success of daughters but not sons. These interactions were unaffected by sleep deprivation.ConclusionsThe direction of the transgenerational effects was not consistent with that predicted under a scenario of adaptive transgenerational plasticity. Instead, they were indicative of expectations based on terminal investment.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0737-6) contains supplementary material, which is available to authorized users.

Maternal Environment Influences Propagule Pressure of an Invasive Plant, Raphanus raphanistrum (Brassicaceae)

Premise of research. Weedy species that invade new areas may experience shifts in environmental conditions across generations. Since maternal environments can significantly influence embryo development, shifts in maternal environments could alter the ability of offspring to colonize.Methodology. Here, we report the results of a set of field experiments that study adaptive transgenerational plasticity across three generations using the agricultural, annual weed, Raphanus raphanistrum. We grew replicate lineages across a gradient of experimentally manipulated soil moisture conditions (control rain [×2], no rain, double normal precipitation) for two generations (maternal and offspring) and transplanted individuals of each population to manipulated or unmanipulated soil moisture conditions. We then measured the consequences of the maternal and offspring soil moisture manipulations on traits critical for weediness in the second generation of plants and third (grandchild) generation of seeds.Pivotal results. Maternal moisture environments significantly influenced offspring development. Offspring of parents from relatively dry environments were significantly smaller (reduced seed biomass, floral displays, and size at reproduction) and less fecund, while offspring of parents from relatively wet environments were significantly larger and more fecund compared with related offspring whose parents had been grown under control moisture conditions. The relative differences among lines grown under various maternal environments were intensified when they were grown in a common environment.Conclusions. Weediness is a product of the population genetics of colonists and environmental characteristics of the invaded environment. Plastic responses to abiotic variation experienced by the maternal parent or offspring may also influence the outcome of dispersal, potentially increasing the relative rate of movement or propagule pressure from relatively wet maternal habitats to dry recipient habitats. Possible implications of these environmentally induced phenotypes are discussed with respect to ecological distribution, persistence under novel environments, and evolution in natural populations.

Grandparental effects in marine sticklebacks: transgenerational plasticity across multiple generations.

Nongenetic inheritance mechanisms such as transgenerational plasticity (TGP) can buffer populations against rapid environmental change such as ocean warming. Yet, little is known about how long these effects persist and whether they are cumulative over generations. Here, we tested for adaptive TGP in response to simulated ocean warming across parental and grandparental generations of marine sticklebacks. Grandparents were acclimated for two months during reproductive conditioning, whereas parents experienced developmental acclimation, allowing us to compare the fitness consequences of short-term vs. prolonged exposure to elevated temperature across multiple generations. We found that reproductive output of F1 adults was primarily determined by maternal developmental temperature, but carry-over effects from grandparental acclimation environments resulted in cumulative negative effects of elevated temperature on hatching success. In very early stages of growth, F2 offspring reached larger sizes in their respective paternal and grandparental environment down the paternal line, suggesting that other factors than just the paternal genome may be transferred between generations. In later growth stages, maternal and maternal granddam environments strongly influenced offspring body size, but in opposing directions, indicating that the mechanism(s) underlying the transfer of environmental information may have differed between acute and developmental acclimation experienced by the two generations. Taken together, our results suggest that the fitness consequences of parental and grandparental TGP are highly context dependent, but will play an important role in mediating some of the impacts of rapid climate change in this system.

Weak evidence for anticipatory parental effects in plants and animals

The evolution of adaptive phenotypic plasticity relies on the presence of cues that enable organisms to adjust their phenotype to match local conditions. Although mostly studied with respect to nonsocial cues, it is also possible that parents transmit information about the environment to their offspring. Such 'anticipatory parental effects' or 'adaptive transgenerational plasticity' can have important consequences for the dynamics and adaptive potential of populations in heterogeneous environments. Yet, it remains unknown how widespread this form of plasticity is. Using a meta-analysis of experimental studies with a fully factorial design, we show that there is only weak evidence for higher offspring performance when parental and offspring environments are matched compared with when they are mismatched. Estimates of heterogeneity among studies suggest that effects, when they occur, are subtle. Study features, environmental context, life stage and trait categories all failed to explain significant amounts of variation in effect sizes. We discuss theoretical and methodological reasons for the limited evidence for anticipatory parental effects and suggest ways to improve our understanding of the prevalence of this form of plasticity in nature.

Drought-induced trans-generational tradeoff between stress tolerance and defence: consequences for range limits?

Areas just across species range boundaries are often stressful, but even with ample genetic variation within and among range-margin populations, adaptation towards stress tolerance across range boundaries often does not occur. Adaptive trans-generational plasticity should allow organisms to circumvent these problems for temporary range expansion; however, range boundaries often persist. To investigate this dilemma, we drought stressed a parent generation of Boechera stricta (A.Gray) A. Löve & D. Löve, a perennial wild relative of Arabidopsis, representing genetic variation within and among several low-elevation range margin populations. Boechera stricta is restricted to higher, moister elevations in temperate regions where generalist herbivores are often less common. Previous reports indicate a negative genetic correlation (genetic tradeoff) between chemical defence allocation and abiotic stress tolerance that may prevent the simultaneous evolution of defence and drought tolerance that would be needed for range expansion. In growth chamber experiments, the genetic tradeoff became undetectable among offspring sib-families whose parents had been drought treated, suggesting that the stress-induced trans-generational plasticity may circumvent the genetic tradeoff and thus enable range expansion. However, the trans-generational effects also included a conflict between plastic responses (environmental tradeoff); offspring whose parents were drought treated were more drought tolerant, but had lower levels of glucosinolate toxins that function in defence against generalist herbivores. We suggest that either the genetic or environmental tradeoff between defence allocation and stress tolerance has the potential to contribute to range limit development in upland mustards.

Adaptive Transgenerational Plasticity in an Annual Plant: Grandparental and Parental Drought Stress Enhance Performance of Seedlings in Dry Soil

Stressful parental (usually maternal) environments can dramatically influence expression of traits in offspring, in some cases resulting in phenotypes that are adaptive to the inducing stress. The ecological and evolutionary impact of such transgenerational plasticity depends on both its persistence across generations and its adaptive value. Few studies have examined both aspects of transgenerational plasticity within a given system. Here we report the results of a growth-chamber study of adaptive transgenerational plasticity across two generations, using the widespread annual plant Polygonum persicaria as a naturally evolved model system. We grew five inbred Polygonum genetic lines in controlled dry vs. moist soil environments for two generations in a fully factorial design, producing replicate individuals of each genetic line with all permutations of grandparental and parental environment. We then measured the effects of these two-generational stress histories on traits critical for functioning in dry soil, in a third (grandchild) generation of seedling offspring raised in the dry treatment. Both grandparental and parental moisture environment significantly influenced seedling development: seedlings of drought-stressed grandparents or parents produced longer root systems that extended deeper and faster into dry soil compared with seedlings of the same genetic lines whose grandparents and/or parents had been amply watered. Offspring of stressed individuals also grew to a greater biomass than offspring of nonstressed parents and grandparents. Importantly, the effects of drought were cumulative over the course of two generations: when both grandparents and parents were drought-stressed, offspring had the greatest provisioning, germinated earliest, and developed into the largest seedlings with the most extensive root systems. Along with these functionally appropriate developmental effects, seedlings produced after two previous drought-stressed generations had significantly greater survivorship in very dry soil than did seedlings with no history of drought. These findings show that plastic responses to naturalistic resource stresses experienced by grandparents and parents can "preadapt" offspring for functioning under the same stresses in ways that measurably influence realized fitness. Possible implications of these environmentally-induced, inherited adaptations are discussed with respect to ecological distribution, persistence under novel stresses, and evolution in natural populations.