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.

     

Multiple simultaneous treatments change plant response from adaptive parental effects to within‐generation plasticity,in Arabidopsis thaliana

In general, studies on plant phenotypic plasticity concentrate on plant responses to different levels of a single environmental factor. Under natural conditions, however, multiple environmental factors often vary simultaneously. I studied the consequences for lifetime fitness caused by single treatments or treatment combinations by investigating patterns of phenotypic plasticity within and between generations. The parental plants (three genotypes of the annual plant Arabidopsis thaliana) received zero, one or two stress treatments at an early life‐stage. The treatments included wounding, shading, chilling, and their pairwise combinations. In the second generation, offspring of treated plants received either the parental or no treatment. Offspring of non‐treated plants were reared under all treatment conditions. Plants responded strongly to the treatments, especially through delayed reproduction, which positively affected lifetime fitness. Notably, treatment combinations triggered stronger plastic responses on average. Because the delay in reproduction was offset by a delay in senescence, the treatments resulted in a fitness gain instead of a loss. However, under adverse environmental conditions, this delay represents a potential fitness cost, especially when the time for reproduction is limited. The treatments ‘wounding’ and ‘shading’ triggered parental effects that increased fitness only in plants that themselves received the treatment. Untreated offspring of wounded or shaded parents performed like control plants. Also, these parental effects were not accompanied by potential fitness costs, such as delayed reproduction. Chilling triggered genotype‐specific parental effects that increased or reduced fitness. Of the treatment combinations only ‘wounding’ and ‘shading’ resulted in genotype‐specific parental effects that increased or reduced fitness independently of offspring treatment. These results suggest that the response of annual plants to treatment combinations triggers predominantly within‐generation plastic responses that include potential fitness costs, which cannot be inferred from studies that manipulate environmental factors individually. Therefore, single treatment studies likely underestimate the costs of plasticity in natural environments.     

Transgenerational plasticity of inducible defences: Combined effects of grand‐parental,parental and current environments

Phenotypic plasticity can occur across generations (transgenerational plasticity) when environments experienced by the previous generations influenced offspring phenotype. The evolutionary importance of transgenerational plasticity, especially regarding within‐generational plasticity, is a currently hot topic in the plasticity framework. How long an environmental effect can persist across generations and whether multigenerational effects are cumulative are primordial—for the evolutionary significance of transgenerational plasticity—but still unresolved questions. In this study, we investigated how the grand‐parental, parental and offspring exposures to predation cues shape the predator‐induced defences of offspring in the Physa acuta snail. We expected that the offspring phenotypes result from a three‐way interaction among grand‐parental, parental and offspring environments. We exposed three generations of snails without and with predator cues according to a full factorial design and measured offspring inducible defences. We found that both grand‐parental and parental exposures to predator cues impacted offspring antipredator defences, but their effects were not cumulative and depended on the defences considered. We also highlighted that the grand‐parental environment did alter reaction norms of offspring shell thickness, demonstrating an interaction between the grand‐parental transgenerational plasticity and the within‐generational plasticity. We concluded that the effects of multigenerational exposure to predator cues resulted on complex offspring phenotypic patterns which are difficult to relate to adaptive antipredator advantages.     

Evidence of adaptive divergence in plasticity: density- and site-dependent selection on shade-avoidance responses in Impatiens capensis

We investigated the conditions under which plastic responses to density are adaptive in natural populations of Impatiens capensis and determined whether plasticity has evolved differently in different selective environments. Previous studies showed that a population that evolved in a sunny site exhibited greater plasticity in response to density than did a population that evolved in a woodland site. Using replicate inbred lines in a reciprocal transplant that included a density manipulation, we asked whether such population differentiation was consistent with the hypothesis of adaptive divergence. We hypothesized that plasticity would be more strongly favored in the sunny site than in the woodland site; consequently, we predicted that selection would be more strongly density dependent in the sunny site, favoring the phenotype that was expressed at each density. Selection on internode length and flowering date was consistent with the hypothesis of adaptive divergence in plasticity. Few costs or benefits of plasticity were detected independently from the expressed phenotype, so plasticity was selected primarily through selection on the phenotype. Correlations between phenotypes and their plasticity varied with the environment and would cause indirect selection on plasticity to be environment dependent. We showed that an appropriate plastic response even to a rare environment can greatly increase genotypic fitness when that environment is favorable. Selection on the measured characters contributed to local adaptation and fully accounted for fitness differences between populations in all treatments except the woodland site at natural density.     

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.     

Adaptive maternal behavioral plasticity and developmental programming mitigate the transgenerational effects of temperature in dung beetles

Phenotypic plasticity allows organisms to cope with rapid environmental change. Yet exactly when during ontogeny plastic responses are elicited, whether plastic responses produced in one generation influence phenotypic variation and fitness in subsequent generations, and the role of plasticity in shaping population divergences, remains overall poorly understood. Here, we use the dung beetle Onthophagus taurus to assess plastic responses to temperature at several life stages bridging three generations and compare these responses across three recently diverged populations. We find that beetles reared at hotter temperatures grow less than those reared at mild temperatures, and that this attenuated growth has transgenerational consequences by reducing offspring size and survival in subsequent generations. However, we also find evidence that plasticity may mitigate these consequences in two ways: 1) mothers modify the temperature of their offspring's developmental environment via behavioral plasticity and 2) in one population, offspring exhibit accelerated growth when exposed to hot temperatures during very early development (‘developmental programming’). Lastly, our study reveals that offspring responses to temperature diverged among populations in fewer than 100 generations, possibly in response to range‐specific changes in climatic or social conditions.     

Phenotypic plasticity for plant development, function and life history

A single genotype can produce different phenotypes in different environments. This fundamental property of organisms is known as phenotypic plasticity. Recently, intensive study has shown that plants are plastic for a remarkable array of ecologically important traits, ranging from diverse aspects of morphology and physiology to anatomy, developmental and reproductive timing, breeding system, and offspring developmental patterns. Comparative, quantitative genetics and molecular approaches are leading to new insights into the adaptive nature of plasticity, its underlying mechanisms and its role in the ecological distribution and evolutionary diversification of plants.     

Cross-generational environmental effects and the evolution of offspring size in the Trinidadian guppy Poecilia reticulata

Abstract The existence of adaptive phenotypic plasticity demands that we study the evolution of reaction norms, rather than just the evolution of fixed traits. This approach requires the examination of functional relationships among traits not only in a single environment but across environments and between traits and plasticity itself. In this study, I examined the interplay of plasticity and local adaptation of offspring size in the Trinidadian guppy, Poecilia reticulata. Guppies respond to food restriction by growing and reproducing less but also by producing larger offspring. This plastic difference in offspring size is of the same order of magnitude as evolved genetic differences among populations. Larger offspring sizes are thought to have evolved as an adaptation to the competitive environment faced by newborn guppies in some environments. If plastic responses to maternal food limitation can achieve the same fitness benefit, then why has guppy offspring size evolved at all? To explore this question, I examined the plastic response to food level of females from two natural populations that experience different selective environments. My goals were to examine whether the plastic responses to food level varied between populations, test the consequences of maternal manipulation of offspring size for offspring fitness, and assess whether costs of plasticity exist that could account for the evolution of mean offspring size across populations. In each population, full‐sib sisters were exposed to either a low‐ or high‐food treatment. Females from both populations produced larger, leaner offspring in response to food limitation. However, the population that was thought to have a history of selection for larger offspring was less plastic in its investment per offspring in response to maternal mass, maternal food level, and fecundity than the population under selection for small offspring size. To test the consequences of maternal manipulation of offspring size for offspring fitness, I raised the offspring of low‐ and high‐food mothers in either low‐ or high‐food environments. No maternal effects were detected at high food levels, supporting the prediction that mothers should increase fecundity rather than offspring size in noncompetitive environments. For offspring raised under low food levels, maternal effects on juvenile size and male size at maturity varied significantly between populations, reflecting their initial differences in maternal manipulation of offspring size; nevertheless, in both populations, increased investment per offspring increased offspring fitness. Several correlates of plasticity in investment per offspring that could affect the evolution of offspring size in guppies were identified. Under low‐food conditions, mothers from more plastic families invested more in future reproduction and less in their own soma. Similarly, offspring from more plastic families were smaller as juveniles and female offspring reproduced earlier. These correlations suggest that a fixed, high level of investment per offspring might be favored over a plastic response in a chronically low‐resource environment or in an environment that selects for lower reproductive effort     

The thrifty phenotype as an adaptive maternal effect

Human diseases in adulthood are increasingly associated with growth patterns in early life, implicating early-life nutrition as the underlying mechanism. The thrifty phenotype hypothesis proposed that early-life metabolic adaptations promote survival, with the developing organism responding to cues of environmental quality by selecting an appropriate trajectory of growth. Recently, some authors have proposed that the thrifty phenotype is also adaptive in the longer-term, by preparing the organism for its likely adult environment. However, windows of plasticity close early during human development, and subsequent environmental changes may result in the selected trajectory becoming inappropriate, leading to adverse effects on health. This paradox generates uncertainty as to whether the thrifty phenotype is indeed adaptive for the offspring in humans. The thrifty phenotype should not be considered a dichotomous concept, rather it refers to the capacity of all offspring to respond to environmental information during early ontogenetic development. This article argues that the thrifty phenotype is the consequence of three different adaptive processes - niche construction, maternal effects, and developmental plasticity - all of which in humans are influenced by our large brains. While developmental plasticity represents an adaptation by the offspring, both niche construction and parental effects are subject to selection on parental rather than offspring fitness. The three processes also operate at different paces. Human offspring do not become net calories-producers until around 18 years of age, such that the high energy costs of the human brain are paid primarily by the mother, even after weaning. The evolutionary expansion of human brain volume occurred in environments characterised by high volatility, inducing strong selective pressure on maternal capacity to provision multiple offspring simultaneously. The thrifty phenotype is therefore best considered as a manipulation of offspring phenotype for the benefit of maternal fitness. The information that enters offspring phenotype during early development does not predict the likely future environment of the offspring, but rather reflects the mother's own developmental experience and the quality of the environment during her own maturation. Offspring growth trajectory thus becomes aligned with long-term maternal capacity to provision. In contemporary populations, the sensitivity of offspring development to maternal phenotype exposes the offspring to adverse effects, through four distinct pathways. The offspring may be exposed to (1) poor maternal metabolic control (e.g. gestational diabetes), (2) maternally derived toxins (e.g. maternal smoking), or (3) low maternal social status (e.g. small size). Adverse consequences of these effects may then be exacerbated by (4) exposure either to the "toxic" western environment in postnatal life, in which diet and physical activity levels are mismatched with metabolic experience in utero, or at the other extreme to famine. The rapid emergence of the epidemic of the metabolic syndrome in the 20th Century reflects the rapid acceleration in the pace of niche construction relative to the slower physiological combination of developmental plasticity and parental effects.     

A unified approach to the evolutionary consequences of genetic and nongenetic inheritance

Inheritance-the influence of ancestors on the phenotypes of their descendants-translates natural selection into evolutionary change. For the past century, inheritance has been conceptualized almost exclusively as the transmission of DNA sequence variation from parents to offspring in accordance with Mendelian rules, but advances in cell and developmental biology have now revealed a rich array of inheritance mechanisms. This empirical evidence calls for a unified conception of inheritance that combines genetic and nongenetic mechanisms and encompasses the known range of transgenerational effects, including the transmission of genetic and epigenetic variation, the transmission of plastic phenotypes (acquired traits), and the effects of parental environment and genotype on offspring phenotype. We propose a unified theoretical framework based on the Price equation that can be used to model evolution under an expanded inheritance concept that combines the effects of genetic and nongenetic inheritance. To illustrate the utility and generality of this framework, we show how it can be applied to a variety of scenarios, including nontransmissible environmental noise, maternal effects, indirect genetic effects, transgenerational epigenetic inheritance, RNA-mediated inheritance, and cultural inheritance.     

Plastic inducible morphologies are not always adaptive: The importance of time delays in a stochastic environment

Summary We present a mathematical model for predicting the expected fitness of phenotypically plastic organisms experiencing a variable environment. We assume that individuals experience two discrete environments probabilistically in time (as a Markov process) and that there are two different phenotypic states, each yielding the highest fitness in one of the two environments. We compare the expected fitness of a phenotypically fixed individual to that of an individual whose phenotype is induced to produce the better phenotype in each environment with a time lag between experiencing a new environment and realization of the new phenotype. Such time lags are common in organisms where phenotypically plastic, inducible traits have been documented. We find that although plasticity is generally adaptive when time lags are short (relative to the time scale of environmental variability), plasticity can be disadvantageous for longer lag times. Asymmetries in environmental change probabilities and/or the relative fitnesses of each phenotype strongly influence whether plasticity is favoured. In contrast to other models, our model does not require costs for plasticity to be disadvantageous; costs affect the results quantitatively, not qualitatively.     

Error management theory and the adaptive significance of transgenerational maternal‐stress effects on offspring phenotype

It is well established that circulating maternal stress hormones (glucocorticoids, GCs) can alter offspring phenotype. There is also a growing body of empirical work, within ecology and evolution, indicating that maternal GCs link the environment experienced by the mother during gestation with changes in offspring phenotype. These changes are considered to be adaptive if the maternal environment matches the offspring's environment and maladaptive if it does not. While these ideas are conceptually sound, we lack a testable framework that can be used to investigate the fitness costs and benefits of altered offspring phenotypes across relevant future environments. We present error management theory as the foundation for a framework that can be used to assess the adaptive potential of maternal stress hormones on offspring phenotype across relevant postnatal scenarios. To encourage rigorous testing of our framework, we provide field‐testable hypotheses regarding the potential adaptive role of maternal stress across a diverse array of taxa and life histories, as well as suggestions regarding how our framework might provide insight into past, present, and future research. This perspective provides an informed lens through which to design and interpret experiments on the effects of maternal stress, provides a framework for predicting and testing variation in maternal stress across and within taxa, and also highlights how rapid environmental change that induces maternal stress may lead to evolutionary traps.     

Maternal effects in the soft scale insect Saissetia coffeae (Hemiptera: Coccidae)

Effects of maternal environment on offspring performance have been documented frequently in herbivorous insects. Despite this, very few cases exist in which exposure of parent insects to a resource causes the phenotype of their offspring to be adjusted in a manner that is adaptive for that resource, a phenomenon called adaptive transgenerational phenotypic plasticity. I performed a two-generation reciprocal cross-transplant experiment in the field with the soft scale insect Saissetia coffeae (Hemiptera: Coccidae) on two disparate host plant species in order to separate genetic effects from possible transgenerational plasticity. Despite striking differences in quality between host species, maternal host had no effect on overall offspring performance, and I detected no "acclimatization" to the maternal host species. However, there was a significant negative association between maternal and offspring development times, with potentially adaptive implications. Furthermore, offspring of mothers reared in an environment where scale densities were higher and scales were more frequently killed by fungi were significantly less likely to suffer from fungal attack than were offspring of mothers reared in an environment where densities were low and fungal attack was rare. Although S. coffeae does not appear to alter offspring phenotype to increase offspring fitness on these two distinct plant species, it does appear that offspring phenotype may be responding to some subtler aspects of maternal environment. In particular, the possibility of induced transgenerational prophylaxis in S. coffeae deserves further investigation.     

Detection vs. selection: integration of genetic,epigenetic and environmental cues in fluctuating environments

There are many inputs during development that influence an organism's fit to current or upcoming environments. These include genetic effects, transgenerational epigenetic influences, environmental cues and developmental noise, which are rarely investigated in the same formal framework. We study an analytically tractable evolutionary model, in which cues are integrated to determine mature phenotypes in fluctuating environments. Environmental cues received during development and by the mother as an adult act as detection‐based (individually observed) cues. The mother's phenotype and a quantitative genetic effect act as selection‐based cues (they correlate with environmental states after selection). We specify when such cues are complementary and tend to be used together, and when using the most informative cue will predominate. Thus, we extend recent analyses of the evolutionary implications of subsets of these effects by providing a general diagnosis of the conditions under which detection and selection‐based influences on development are likely to evolve and coexist.     

Phenotypic and transgenerational plasticity promote local adaptation to sun and shade environments

Adaptive plasticity is expected to be important when the grain of environmental variation is encompassed in offspring dispersal distance. We investigated patterns of local adaptation, selection and plasticity in an association of plant morphology with fine-scale habitat shifts from oak canopy understory to adjacent grassland habitat in Claytonia perfoliata. Populations from beneath the canopy of oak trees were >90 % broad leaved and large seeded, while plants from adjacent grassland habitat were >90 % linear-leaved and small seeded. In a 2-year study, we used reciprocal transplants and phenotypic selection analysis to investigate local adaptation, selection, plasticity and maternal effects in this trait-environment association. Transgenerational effects were studied by planting offspring of inbred maternal families grown in both environments across the same environments in the second year. Reciprocal transplants revealed local adaptation to habitat type: broad-leaved forms had higher fitness in oak understory and linear-leaved plants had higher fitness in open grassland habitat. Phenotypic selection analyses indicated selection for narrower leaves and lower SLA in open habitat, and selection for broad leaves and intermediate values of SLA in understory. Both plant morphs exhibited plastic responses in traits in the same direction as selection on traits (narrower leaves and lower SLA in open habitat) suggesting that plasticity is adaptive. We detected an adaptive transgenerational effect in which maternal environment influenced offspring fitness; offspring of grassland-reared plants had higher fitness than understory-reared plants when grown in grassland. We did not detect costs of plasticity, but did find a positive association between leaf shape plasticity and fitness in linear-leaved plants in grassland habitat. Together, these findings indicate that fixed differences in trait values corresponding to selection across habitat contribute to local adaptation, but that plasticity and maternal environmental effects may be favored through promotion of survival across heterogeneous 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.     

Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity

Young vertebrates have limited capacity to synthesize antibodies and are dependent on the protection of maternally transmitted antibodies for humoral disease resistance early in life. However, mothers may enhance fitness by priming their offspring's immune systems to elevate disease resistance. Transgenerational induced defences have been documented in plants and invertebrates, but maternal priming of offspring immunity in vertebrates has been essentially neglected. To test the ability of mothers to stimulate the immune systems of offspring, we manipulated maternal and offspring antigen exposure in a wild population of birds, pied flycatchers (Ficedula hypoleuca). We show that immunization of the mother before egg laying apparently stimulates a transgenerational defence against pathogens by elevating endogenous offspring antibody production. If the disease environments encountered by mothers and offspring are similar, this transgenerational immune priming may allow young to better cope with the local pathogen fauna.     

Rapid within‐ and transgenerational changes in thermal tolerance and fitness in variable thermal landscapes

Phenotypic plasticity may increase the performance and fitness and allow organisms to cope with variable environmental conditions. We studied within‐generation plasticity and transgenerational effects of thermal conditions on temperature tolerance and demographic parameters in Drosophila melanogaster. We employed a fully factorial design, in which both parental (P) and offspring generations (F1) were reared in a constant or a variable thermal environment. Thermal variability during ontogeny increased heat tolerance in P, but with demographic cost as this treatment resulted in substantially lower survival, fecundity, and net reproductive rate. The adverse effects of thermal variability (V) on demographic parameters were less drastic in flies from the F1, which exhibited higher net reproductive rates than their parents. These compensatory responses could not totally overcome the challenges of the thermally variable regime, contrasting with the offspring of flies raised in a constant temperature (C) that showed no reduction in fitness with thermal variation. Thus, the parental thermal environment had effects on thermal tolerance and demographic parameters in fruit fly. These results demonstrate how transgenerational effects of environmental conditions on heat tolerance, as well as their potential costs on other fitness components, can have a major impact on populations’ resilience to warming temperatures and more frequent thermal extremes.     

Who listens to mother? A whole-family perspective on the evolution of maternal hormone allocation

Maternal effects, or the influence of maternal environment and phenotype on offspring phenotype, may allow mothers to fine-tune their offspring's developmental trajectory and resulting phenotype sometimes long after the offspring has reached independence. However, maternal effects on offspring phenotype do not evolve in isolation, but rather within the context of a family unit, where the separate and often conflicting evolutionary interests of mothers, fathers and offspring are all at play. While intrafamilial conflicts are routinely invoked to explain other components of reproductive strategy, remarkably little is known about how intrafamilial conflicts influence maternal effects. We argue that much of the considerable variation in the relationship between maternally derived hormones, nutrients and other compounds and the resulting offspring phenotype might be explained by the presence of conflicting selection pressures on different family members. In this review, we examine the existing literature on maternal hormone allocation as a case study for maternal effects more broadly, and explore new hypotheses that arise when we consider current findings within a framework that explicitly incorporates the different evolutionary interests of the mother, her offspring and other family members. Specifically, we hypothesise that the relationship between maternal hormone allocation and offspring phenotype depends on a mother's ability to manipulate the signals she sends to offspring, the ability of family members to be plastic in their response to those signals and the capacity for the phenotypes and strategies of various family members to interact and influence one another on both behavioural and evolutionary timescales. We also provide suggestions for experimental, comparative and theoretical work that may be instrumental in testing these hypotheses. In particular, we highlight that manipulating the level of information available to different family members may reveal important insights into when and to what extent maternal hormones influence offspring development. We conclude that the evolution of maternal hormone allocation is likely to be shaped by the conflicting fitness optima of mothers, fathers and offspring, and that the outcome of this conflict depends on the relative balance of power between family members. Extending our hypotheses to incorporate interactions between family members, as well as more complex social groups and a wider range of taxa, may provide exciting new developments in the fields of endocrinology and maternal effects.     

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.