Transgenerational effects of stress exposure on offspring phenotypes in apomictic dandelion

Heritable epigenetic modulation of gene expression is a candidate mechanism to explain parental environmental effects on offspring phenotypes, but current evidence for environment-induced epigenetic changes that persist in offspring generations is scarce. In apomictic dandelions, exposure to various stresses was previously shown to heritably alter DNA methylation patterns. In this study we explore whether these induced changes are accompanied by heritable effects on offspring phenotypes. We observed effects of parental jasmonic acid treatment on offspring specific leaf area and on offspring interaction with a generalist herbivore; and of parental nutrient stress on offspring root-shoot biomass ratio, tissue P-content and leaf morphology. Some of the effects appeared to enhance offspring ability to cope with the same stresses that their parents experienced. Effects differed between apomictic genotypes and were not always consistently observed between different experiments, especially in the case of parental nutrient stress. While this context-dependency of the effects remains to be further clarified, the total set of results provides evidence for the existence of transgenerational effects in apomictic dandelions. Zebularine treatment affected the within-generation response to nutrient stress, pointing at a role of DNA methylation in phenotypic plasticity to nutrient environments. This study shows that stress exposure in apomictic dandelions can cause transgenerational phenotypic effects, in addition to previously demonstrated transgenerational DNA methylation effects.     

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.     

Clonal Transgenerational Effects Transmit for Multiple Generations in a Floating Plant

Environmental conditions of a parent plant can influence the performance of their clonal offspring, and such clonal transgenerational effects may help offspring adapt to different environments. However, it is still unclear how many vegetative generations clonal transgenerational effects can transmit for and whether it depends on the environmental conditions of the offspring. We grew the ancestor ramets of the floating clonal plant Spirodela polyrhiza under a high and a low nutrient level and obtained the so-called 1^st-generation offspring ramets of two types (from these two environments). Then we grew the 1^st-generation offspring ramets of each type under the high and the low nutrient level and obtained the so-called 2^nd-generation offspring ramets of four types. We repeated this procedure for another five times and analyzed clonal transgenerational effects on growth, morphology and biomass allocation of the 1^st- to the 6^th-generation offspring ramets. We found positive, negative or neutral (no) transgenerational effects of the ancestor nutrient condition on the offspring of S. polyrhiza, depending on the number of vegetative generations, the nutrient condition of the offspring environment and the traits considered. We observed significant clonal transgenerational effects on the 6^th-generation offspring; such effects occurred for all three types of traits (growth, morphology and allocation), but varied depending on the nutrient condition of the offspring environment and the traits considered. Our results suggest that clonal transgenerational effects can transmit for multiple vegetative generations and such impacts can vary depending on the environmental conditions of offspring.     

Salinity Adaptation and the Contribution of Parental Environmental Effects in Medicago truncatula

High soil salinity negatively influences plant growth and yield. Some taxa have evolved mechanisms for avoiding or tolerating elevated soil salinity, which can be modulated by the environment experienced by parents or offspring. We tested the contribution of the parental and offspring environments on salinity adaptation and their potential underlying mechanisms. In a two-generation greenhouse experiment, we factorially manipulated salinity concentrations for genotypes of Medicago truncatula that were originally collected from natural populations that differed in soil salinity. To compare population level adaptation to soil salinity and to test the potential mechanisms involved we measured two aspects of plant performance, reproduction and vegetative biomass, and phenological and physiological traits associated with salinity avoidance and tolerance. Saline-origin populations had greater biomass and reproduction under saline conditions than non-saline populations, consistent with local adaptation to saline soils. Additionally, parental environmental exposure to salt increased this difference in performance. In terms of environmental effects on mechanisms of salinity adaptation, parental exposure to salt spurred phenological differences that facilitated salt avoidance, while offspring exposure to salt resulted in traits associated with greater salt tolerance. Non-saline origin populations expressed traits associated with greater growth in the absence of salt while, for saline adapted populations, the ability to maintain greater performance in saline environments was also associated with lower growth potential in the absence of salt. Plastic responses induced by parental and offspring environments in phenology, leaf traits, and gas exchange contribute to salinity adaptation in M. truncatula. The ability of plants to tolerate environmental stress, such as high soil salinity, is likely modulated by a combination of parental effects and within-generation phenotypic plasticity, which are likely to vary in populations from contrasting environments.     

The role of transgenerational effects in adaptation of clonal offspring of white clover (<Emphasis Type="Italic">Trifolium repens</Emphasis>) to drought and herbivory

Environmentally induced transgenerational effects can increase success of offspring and thereby be adaptive if offspring experience conditions similar to the parental environment. The ecological and evolutionary significance of these effects in plants have been considered overwhelmingly in the context of sexual generations. We investigated whether drought stress and jasmonic acid, a key hormone involved in induction of plant defenses against herbivores, applied in the parental generation, trigger transgenerational effects in clonal offspring of Trifolium repens and whether these effects are adaptive. We found that drought stress experienced by parents significantly affected phenotypes of offspring ramets. Offspring ramets were bigger if they were produced in the parental water regime (control/drought). Repeated application of jasmonic acid to parents increased the subsequent growth of offspring ramets produced by stolons after they were disconnected from the parental clone. However, these offspring ramets experienced similar herbivory by the generalist Spodoptera littoralis caterpillar as did control offspring ramets, indicating that this jasmonic acid application in the parental generation did not result in a transgenerational effect comprising increased herbivory resistance. We conclude that, overall, environmental interaction in the parental generation can trigger transgenerational effects in clonal plants and some of these effects can be adaptive. Moreover, transgenerational effects in clonal plants that significantly influence their growth and behavior can ultimately affect the evolutionary trajectories of clonal populations.     

Environmental enrichment induces intergenerational behavioural and epigenetic effects on fish

Parental effects influence offspring phenotypes through pre‐ and post‐natal routes but little is known about their molecular basis, and therefore their adaptive significance. Epigenetic modifications, which control gene expression without changes in the DNA sequence and are influenced by the environment, may contribute to parental effects. We investigated the effects of environmental enrichment on the behaviour, metabolic rate and brain DNA methylation patterns of parents and offspring of the highly inbreed mangrove killifish (Kryptolebias marmoratus). Parental fish reared in enriched environments had lower cortisol levels, lower metabolic rates and were more active and neophobic than those reared in barren environments. They also differed in 1,854 methylated cytosines (DMCs). Offspring activity and neophobia were determined by the parental environment. Among the DMCs of the parents, 98 followed the same methylation patterns in the offspring, three of which were significantly influenced by parental environments irrespective of their own rearing environment. Our results suggest that parental environment influences the behaviour and, to some extent, the brain DNA methylation patterns of the offspring.     

Effects of maternal and grandmaternal flea infestation on offspring quality and quantity in a desert rodent: evidence for parasite-mediated transgenerational phenotypic plasticity

Parasites can cause a broad range of sublethal fitness effects across a wide variety of host taxa. However, a host’s efforts to compensate for possible parasite-induced fitness effects are less well-known. Parental effects may beneficially alter the offspring phenotype if parental environments sufficiently predict the offspring environment. Parasitism is a common stressor across generations; therefore, parental infestation could reliably predict the likelihood of infestation for offspring. However, little is known about relationships between parasitism and transgenerational phenotypic plasticity. Thus, we investigated how maternal and grandmaternal infestation with fleas (Xenopsylla ramesis) affected offspring quality and quantity in a desert rodent (Meriones crassus). We used a fully-crossed design with control and infested treatments to examine litter size, pup body mass at birth, and pup mass gain before weaning for combinations of maternal and grandmaternal infestation status. No effect of treatment on litter size or pup body mass at birth was found. However, maternal and grandmaternal infestation status significantly affected pre-weaning body mass gain, a proxy for the rate of maturation, in male pups. Pups gained significantly more weight before weaning if maternal and grandmaternal infestation statuses matched, regardless of the treatment. Thus, pups whose mothers and grandmothers experienced similar risks of parasitism, either both non-parasitized or both infested, would reach sexual maturity more quickly than those pups whose mothers’ infestation status did not match that of their grandmothers. These results support the contention that parents can receive external cues such as the risk of parasitism, that prompt them to alter offspring provisioning. Therefore, parasites could be a mediator of environmentally-induced maternal effects and could affect host reproductive fitness across multiple generations.     

Parasite resistance and parasite tolerance: insights into transgenerational immune priming in an invertebrate host

Parasites impose different selection regimes on their hosts, which respond by increasing their resistance and/or tolerance. Parental challenge with parasites can enhance the immune response of their offspring, a phenomenon documented in invertebrates and termed transgenerational immune priming. We exposed two parental generations of the model organism Daphnia magna to the horizontally transmitted parasitic yeast Metschnikowia bicuspidata and recorded resistance- and tolerance-related traits in the offspring generation. We hypothesized that parentally primed offspring will increase either their resistance or their tolerance to the parasite. Our susceptibility assays revealed no impact of parental exposure on offspring resistance. Nonetheless, different fitness-related traits, which are indicative of tolerance, were altered. Specifically, maternal priming increased offspring production and decreased survival. Grandmaternal priming positively affected age at first reproduction and negatively affected brood size at first reproduction. Interestingly, both maternal and grandmaternal priming significantly reduced within-host–parasite proliferation. Nevertheless, Daphnia primed for two consecutive generations had no competitive advantage in comparison to unprimed ones, implying additive maternal and grandmaternal effects. Our findings do not support evidence of transgenerational immune priming from bacterial infections in the same host species, thus, emphasizing that transgenerational immune responses may not be consistent even within the same host species.     

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.     

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.     

Transgenerational effects of parent and grandparent gender on offspring development in a biparental beetle species

Parental effects on offspring life-history traits are common and increasingly well-studied. However, the extent to which these effects persist into offspring in subsequent generations has received less attention. In this experiment, maternal and paternal effects on offspring and grand-offspring were investigated in the biparental burying beetle Nicrophorus vespilloides, using a split-family design. This allowed the separation of prenatal and postnatal transgenerational effects. Grandparent and parent gender were found to have a cumulative effect on offspring development and may provide a selection pressure on the division of parental investment in biparental species.     

Shaped by the past,acting in the present: transgenerational plasticity of anti‐predatory traits

Phenotypic expression can be altered by direct perception of environmental cues (within‐generation phenotypic plasticity) and by the environmental cues experienced by previous generations (transgenerational plasticity). Few studies, however, have investigated how the characteristics of phenotypic traits affect their propensity to exhibit plasticity within and across generations. We tested whether plasticity differed within and across generations between morphological and behavioral anti‐predator traits of Physa acuta, a freshwater snail. We reared 18 maternal lineages of P. acuta snails over two generations using a full factorial design of exposure to predator or control cues and quantified adult F₂ shell size, shape, crush resistance, and anti‐predator behavior – all traits which potentially affect their ability to avoid or survive predation attempts. We found that most morphological traits exhibited transgenerational plasticity, with parental exposure to predator cues resulting in larger and more crush‐resistant offspring, but shell shape demonstrated within‐generation plasticity. In contrast, we found that anti‐predator behavior expressed only within‐generation plasticity such that offspring reared in predator cues responded less to the threat of predation than control offspring. We discuss the consequences of this variation in plasticity for trait evolution and ecological dynamics. Overall, our study suggests that further empirical and theoretical investigation is needed in what types of traits are more likely to be affected by within‐generational and transgenerational plasticity.     

Parental environmental effects on life history traits in Arabidopsis thaliana (Brassicaceae)

Environmentally induced maternal effects on offspring phenotype are well known in plants. When genotypes or maternal lineages are replicated and raised in different environmental conditions, the phenotype of their offspring often depends on the environment in which the parents developed. However, the degree to which such maternal effects are maintained over subsequent generations has not been documented in many taxa. Here we report the results of a study designed to assess the effects of parental environment on vegetative and reproductive traits, using glasshouse-raised maternal lines sampled from natural populations of Arabidopsis thaliana . Replicates of five highly selfed lines from each of four wild populations were cultivated in two abiotic environments in the glasshouse, and the quality and performance of seeds derived from these two environments were examined over two generations. We found that offspring phenotype was strongly influenced by parental environment, but because the parental environments differed with respect to the time of seed harvest, it was not possible to distinguish clearly between parental environmental effects and the possible (but unlikely) effects of seed age on offspring phenotype. We observed a rapid decline in the expression of ancestral environmental effects, and no main environmental effects on progeny phenotype persisted in the second generation. The mechanism of transmission of environmental effects did not appear to be associated with the quantity or quality of reserves in the seeds, suggesting that environmental effects may be transmitted across subsequent generations via some mechanism that generates environment-specific gene expression.     

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.     

Adaptive transgenerational plasticity in the perennial Plantago lanceolata

Phenotypes of plants, and thus their ecology and evolution, can be affected by the environmental conditions experienced by their parents, a phenomenon called parental effects or transgenerational plasticity. However, whether such effects are just passive responses or represent a special type of adaptive plasticity remains controversial because of a lack of solid tests of their adaptive significance. Here, we investigated transgenerational effects of different nutrient environments on the productivity, carbon storage and flowering phenology of the perennial plant Plantago lanceolata, and whether these effects are influenced by seasonal variation in the maternal environment. We found that maternal environments significantly affected the offspring phenotype, and that plants consistently produced more biomass and had greater root carbohydrate storage if grown under the same environmental conditions as experienced by their mothers. The observed transgenerational effects were independent of the season in which seeds had matured. We therefore conclude that transgenerational effects on biomass and carbon storage in P. lanceolata are adaptive regardless of the season of seed maturation.     

Predator-induced maternal and paternal effects independently alter sexual selection

Parental experience alters survival-related phenotypes of offspring in both adaptive and nonadaptive ways, yielding rapid inter- and transgenerational fitness effects. Yet, fitness comprises survival and reproduction, and parental effects on mating decisions could alter the strength and direction of sexual selection, affecting long-term evolutionary trajectories. We used a full factorial design in which threespine stickleback (Gasterosteus aculeatus) mothers, fathers, both, or neither were exposed to a model predator at developmentally appropriate times to test for predator-induced maternal, paternal, and joint parental effects on daughters’ mating behavior. We tested the responsiveness, preferences, and mate choices of adult daughters in no-choice trials with wild-caught males who had varied sexual signals. Maternal and paternal predator exposure independently yielded daughters who preferred males who were intermediate in conspicuousness (with duller nuptial coloration and who courted less vigorously), relaxing the typical preference for the most conspicuous males. The combined effects of maternal and paternal predator exposure were not cumulative; when both parents were predator exposed, single-parent effects on mate preferences were reversed. Thus, we cannot assume that maternal and paternal effects additively combine to produce “parental” effects. Further, joint parental predator exposure yielded daughters who were three times less likely to mate at all. Stress-induced intergenerational parental effects on reproductive decisions such as those observed here may potentiate rapid transgenerational responses to novel and changing mating environments.     

Epigenetics and parental effects

Parental effects are a major source of phenotypic plasticity and may influence offspring phenotype in concert with environmental demands. Studies of “environmental epigenetics” suggest that (1) DNA methylation states are variable and that both demethylation and remethylation occur in post‐mitotic cells, and (2) that remodeling of DNA methylation can occur in response to environmentally driven intracellular signaling pathways. Studies of mother‐offspring interactions in rodents suggest that parental signals influence the DNA methylation, leading to stable changes in gene expression. If parental effects do indeed enhance the “match” between prevailing environmental demands and offspring phenotype, then the potential for variation in environmental conditions over time would suggest a mechanism that requires active maintenance across generations through parental signaling. We suggest that parental regulation of DNA methylation states is thus an ideal candidate mechanism for parental effects on phenotypic variation.     

Transgenerational effects benefit offspring across diverse environments: a meta‐analysis in plants and animals

The adaptive value of transgenerational effects (the ancestor environmental effects on offspring) in changing environments has received much attention in recent years, but the related empirical evidence remains equivocal. Here, we conducted a meta‐analysis summarising 139 experimental studies in plants and animals with 1170 effect sizes to investigate the generality of transgenerational effects across taxa, traits, and environmental contexts. It was found that transgenerational effects generally enhanced offspring performance in response to both stressful and benign conditions. The strongest effects are in annual plants and invertebrates, whereas vertebrates appear to benefit mostly under benign conditions, and perennial plants show hardly any transgenerational responses at all. These differences among taxonomic/life‐history groups possibly reflect that vertebrates can avoid stressful conditions through their mobility, and longer‐lived plants have alternative strategies. In addition to environmental contexts and taxonomic/life‐history groups, transgenerational effects also varied among traits and developmental stages of ancestors and offspring, but the effects were similarly strong across three generations of offspring. By way of a more comprehensive data set and a different effect size, our results differ from those of a recent meta‐analysis, suggesting that transgenerational effects are widespread, strong and persistent and can substantially impact the responses of plants and animals to changing environments.     

Transgenerational effects of heavy metal pollution on immune defense of the blow fly Protophormia terraenovae

Recently environmental conditions during early parental development have been found to have transgenerational effects on immunity and other condition-dependent traits. However, potential transgenerational effects of heavy metal pollution have not previously been studied. Here we show that direct exposure to heavy metal (copper) upregulates the immune system of the blow fly, Protophormia terraenovae, reared in copper contaminated food. In the second experiment, to test transgenerational effects of heavy metal, the parental generation of the P. terraenovae was reared in food supplemented with copper, and the immunocompetence of their offspring, reared on uncontaminated food, was measured. Copper concentration used in this study was, in the preliminary test, found to have no effect on mortality of the flies. Immunity was tested on the imago stage by measuring encapsulation response against an artificial antigen, nylon monofilament. We found that exposure to copper during the parental development stages through the larval diet resulted in immune responses that were still apparent in the next generation that was not exposed to the heavy metal. We found that individuals reared on copper-contaminated food developed more slowly compared with those reared on uncontaminated food. The treatment groups did not differ in their dry body mass. However, parental exposure to copper did not have an effect on the development time or body mass of their offspring. Our study suggests that heavy metal pollution has positive feedback effect on encapsulation response through generations which multiplies the harmful effects of heavy metal pollution in following generations.     

Effects of parental and own early developmental conditions on the phenotype in zebra finches (Taeniopygia guttata)

The performance of an individual can be critically influenced by its experience early in life as well as trans-generationally by the conditions experienced by its parents. However, it remains unclear whether or not the early experience of parents and offspring interact with each other and adapt offspring when the parental and own early environmental conditions match. Here, zebra finches (Taeniopygia guttata) that had experienced either early low or high nutritional conditions raised their offspring under either matched or mismatched nutritional conditions. Parental and offspring early conditions both separately affected the offspring’s adult phenotype, but early conditions experienced by parents and offspring did not interact as predicted. Offspring that grew up under conditions matching those their parents had experienced did not do better than those that grew up in a mismatched environment. Thus, transgenerational effects remain a lifelong burden to the offspring acting in addition to the offspring’s own early life experience. The lack of evidence for adaptive programming to matching environmental conditions may result from non-predictive environments under natural conditions in such opportunistic breeders.