Transgenerational Adaptation Research Articles

Antibodies in breast milk: Pro-bodies designed for healthy newborn development.

This manuscript sheds light on the impact of maternal breast milk antibodies on infant health. Milk antibodies prepare and protect the newborn against environmental exposure, guide and regulate the offspring's immune system, and promote transgenerational adaptation of the immune system to its environment. While the transfer of IgG across the placenta ceases at birth, milk antibodies are continuously replenished by the maternal immune system. They reflect the mother's real-time adaptation to the environment to which the infant is exposed. They cover the infant's upper respiratory and digestive mucosa and are perfectly positioned to control responses to environmental antigens and might also reach their circulation. Maternal antibodies in breast milk play a key role in the immune defense of the developing child, with a major impact on infectious disease susceptibility in both HIC and LMIC. They also influence the development of another major health burden in children-allergies. Finally, emerging evidence shows that milk antibodies also actively shape immune development. Much of this is likely to be mediated by their effect on the seeding, composition and function of the microbiota, but not only. Further understanding of the bridge that maternal antibodies provide between the child and its environment should enable the best interventions to promote healthy development.

Feeding on stressed algae exerts important effects on life history traits of Daphnia magna in a multi-stressor environment

Freshwater ecosystems are increasingly exposed to anthropogenic eutrophication, including high nitrogen. In addition, climate change is leading to more intense and frequent heatwaves, which have enormous impacts on all trophic levels of the ecosystem. Any change in the lower trophic levels, e.g., the phytoplankton, also introduces stress to higher trophic levels e.g., the zooplankton crustacean Daphnia. Individual effects of heatwaves, high nitrate, and changing feed quality have been studied in daphnia, but less is known about their interactive effects. This study used a 3 × 3 × 2 factorial design in which daphnia were exposed to combinations of ecologically relevant nitrate concentrations (0, 50, or 200 mg/L) and different heatwave scenarios (no, short-moderate, or long-intense) in which individuals were either fed with microalgae (P. subcapitata and C. reinhardtii) grown at 20 °C and 50 mg/L nitrate (control feed) or the same conditions as daphnia was exposed to (experimental feed). Throughout the experiment, the interactive effects of high nitrate, heatwave, and feed on mortality, maturation, offspring, and body size were evaluated. In general, heatwaves shorten the lifespan of daphnia. Exposing daphnia to a long-intense heatwave combined with high nitrate resulted in poor performance. In the nitrate-limited condition, however, the restricted proliferation of microalgae reduced feed availability, which also had a major impact on daphnia's life history traits. Daphnia cultured in high nitrate and fed control feed performed better than when fed experimental feed, suggesting that in a high nitrate condition, the microalgae grown under the same experimental conditions was either unable to meet energy requirements or introduced extra stress for the daphnia. Most importantly, the effect of nitrate and heatwave as stressors on the availability and quality of the feed had a greater impact on daphnia than its direct impact. Interestingly, a transgenerational adaptation to nitrate was observed which may help to maintain ecological balance in the long run.

Transgenerational adaptation to ocean acidification determines the susceptibility of filter-feeding rotifers to nanoplastics

The adaptation of marine organisms to the impending challenges presented by ocean acidification (OA) is essential for their future survival, and mechanisms underlying OA adaptation have been reported in several marine organisms. In the natural environment, however, marine organisms are often exposed to a combination of environmental stressors, and the interactions between adaptive responses have yet to be elucidated. Here, we investigated the susceptibility of filter-feeding rotifers to short-term (ST) and long-term (LT) (≥180 generations) high CO2 conditions coupled with nanoplastic (NPs) exposure (ST+ and LT+). Adaptation of rotifers to elevated CO2 caused differences in ingestion and accumulation of NPs, resulting in a significantly different mode of action on in vivo endpoints between the ST+ and LT+ groups. Moreover, microRNA-mediated epigenetic regulation was strongly correlated with the varied adaptive responses between the ST+ and LT+ groups, revealing novel regulatory targets and pathways. Our results indicate that pre-exposure history to increased CO2 levels is an important factor in the susceptibility of rotifers to NPs.

Transgenerational endocrine disruptor effects of cadmium in zebrafish and contribution of standing epigenetic variation to adaptation

Evidence has emerged that environmentally-induced epigenetic changes can have long-lasting effects on gene transcription across generations. These recent findings highlight the need to investigate the transgenerational impacts of pollutants to assess their long term effects on populations. In this study, we investigated the transgenerational effect of cadmium on zebrafish across 4 generations. A first whole methylome approach carried out on fish of the first two generations led us to focus our investigations on the estradiol receptor alpha gene (esr1). We observed a sex-dependent transgenerational inheritance of Cd-induced DNA methylation changes up to the last generation. These changes were associated with single nucleotide polymorphisms (SNPs) that were themselves at the origin of the creation or deletion of methylation sites. Thus, Cd-induced genetic selection gave rise to DNA methylation changes. We also analyzed the transcription level of various sections of esr1 as well as estrogen responsive genes. While Cd triggered transgenerational disorders, Cd-induced epigenetic changes in esr1 contributed to the rapid transgenerational adaptation of fish to Cd. Our results provide insight into the processes underpinning rapid adaptation and highlight the need to maintain genetic diversity within natural populations to bolster the resilience of species faced with the global environmental changes.

Genetic and epigenetic interplay allows rapid transgenerational adaptation to metal pollution in zebrafish.

Despite still being a matter of debate, there is growing evidence that pollutant-induced epigenetic changes can be propagated across generations. Whereas such modifications could have long-lasting effects on organisms and even on population, environmentally relevant data from long-term exposure combined with follow-up through multiple generations remain scarce for non-mammalian species. We performed a transgenerational experiment comprising four successive generations of zebrafish. Only fish from the first generation were exposed to an environmentally realistic concentration of cadmium (Cd). Using a whole methylome analysis, we first identified the DNA regions that were differentially methylated in response to Cd exposure and common to fish of the first two generations. Among them, we then focused our investigations on the exon 3 (ex3) of the cep19 gene. We indeed recorded transgenerational growth disorders in Cd-exposed fish, and a mutation in this exon is known to cause morbid obesity in mammals. Its methylation level was thus determined in zebrafish from all the four generations by means of a targeted and base resolution method. We observed a transgenerational inheritance of Cd-induced DNA methylation changes up to the fourth generation. However, these changes were closely associated with genetic variations, mainly a single nucleotide polymorphism. This single nucleotide polymorphism was itself at the origin of the creation or deletion of a methylation site and deeply impacted the methylation level of neighboring methylation sites. Cd-induced epigenetic changes were associated with different mRNA transcripts and an improved condition of Cd fish. Our results emphasize a tight relationship between genetic and epigenetic mechanisms and suggest that their interplay and pre-existing diversity can allow rapid adaptation to anthropogenic environmental changes.

Rapid transgenerational adaptation in response to intercropping reduces competition.

By capitalising on positive biodiversity-productivity relationships, intercropping provides opportunities to improve agricultural sustainability. Intercropping is generally implemented using commercial seeds that were bred for maximal productivity in monocultures, thereby ignoring the ability of plants to adapt over generations to the surrounding neighbourhood, notably through increased complementarity, that is reduced competition or increased facilitation. This is why using monoculture-adapted seeds for intercropping might limit the benefits of crop diversity on yield. However, the adaptation potential of crops and the corresponding changes in complementarity have not been explored in annual crop systems. Here we show that plant-plant interactions among annual crops shifted towards reduced competition and/or increased facilitation when the plants were growing in the same community type as their parents did in the previous two generations. Total yield did not respond to this common coexistence history, but in fertilized conditions, we observed increased overyielding in mixtures with a common coexistence history. Surprisingly, we observed character convergence between species sharing the same coexistence history for two generations, in monocultures but also in mixtures: the six crop species tested converged towards taller phenotypes with lower leaf dry matter content. This study provides the first empirical evidence for the potential of parental diversity affecting plant-plant interactions, species complementarity and therefore potentially ecosystem functioning of the following generations in annual cropping systems. Although further studies are required to assess the context-dependence of these results, our findings may still have important implications for diversified agriculture as they illustrate the potential of targeted cultivars to increase complementarity of species in intercropping, which could be achieved through specific breeding for mixtures.

A prenatal acoustic signal of heat affects thermoregulation capacities at adulthood in an arid-adapted bird

Understanding animal physiological adaptations for tolerating heat, and the causes of inter-individual variation, is key for predicting climate change impacts on biodiversity. Recently, a novel mechanism for transgenerational heat adaptation was identified in a desert-adapted bird, where parents acoustically signal hot conditions to embryos. Prenatal exposure to “heat-calls” adaptively alters zebra finch development and their thermal preferences in adulthood, suggesting a long-term shift towards a heat-adapted phenotype. However, whether such acoustic experience improves long-term thermoregulatory capacities is unknown. We measured metabolic rate (MR), evaporative water loss (EWL) and body temperature in adults exposed to a stepped profile of progressively higher air temperatures (Ta) between 27 and 44 °C. Remarkably, prenatal acoustic experience affected heat tolerance at adulthood, with heat-call exposed individuals more likely to reach the highest Ta in morning trials. This was despite MR and EWL reaching higher levels at the highest Ta in heat-call individuals, partly driven by a stronger metabolic effect of moderate activity. At lower Ta, however, heat-call exposed individuals had greater relative water economy, as expected. They also better recovered mass lost during morning trials. We therefore provide the first evidence that prenatal acoustic signals have long-term consequences for heat tolerance and physiological adaptation to heat.

Transgenerational Effect of Drought Stress and Sub-Lethal Doses of Quizalofop-p-ethyl: Decreasing Sensitivity to Herbicide and Biochemical Adjustment in Eragrostis plana

(1) Background: Eragrostis plana Ness is a invasive C4 perennial grass in South America and very adaptable to environmental stresses. Our hypothesis is that there is a transgenerational cross-talk between environmental stresses and weed response to herbicides. This study’s objectives were to: (1) evaluate if E. plana primed by drought stress (DRY), a sub-lethal dose of quizalofop-p-ethyl (QPE), or a combination of both drought and herbicide stresses (DRY × QPE), produce a progeny with decreased sensitivity to quizalofop and (2) investigate the potential mechanisms involved in this adaptation; (2) Methods: A population of E. plana was isolatedly submitted to treatments for drought, quizalofop or drought plus quizalofop for two generations. The progenies were analyzed for sensitivity to the herbicide quizalofop and performed biochemical, chromatographic and molecular analyses.; (3) Results: In the G2 generation, the quizalofop-treated CHK population had reduced stomatal conductance and increased hydrogen peroxide and lipid peroxidation. On the other hand, there was no change in stomatal conductance, hydrogen peroxide level, and lipid peroxidation in the quizalofop-treated DRY population. In addition, this population had increased antioxidant enzyme activity and upregulated CYP72A31 and CYP81A12 expression, which was accompanied by reduced quizalofop-p-ethyl concentrations; (4) Conclusions: E. plana demonstrated a capacity for transgenerational adaptation to abiotic stresses, with the population exposed to drought stress (DRY) becoming less sensitive to quizalofop-p-ethyl treatment.

Seed germination dynamics of silverleaf nightshade (Solanum elaeagnifolium Cav.) and implications for effective weed management

AbstractSilverleaf nightshade (Solanum elaeagnifolium Cav.) is a noxious weed that threatens agricultural productivity and biodiversity worldwide. The long‐term management of soil seedbanks along with the aboveground populations of silverleaf nightshade has the potential to effectively control the species in its introduced range. Implementation of this strategy requires insights into the germination behavior of the weed in response to various environmental stimuli and endogenous cues. We assessed the morphology and germination of silverleaf nightshade seeds from an agricultural farm, native rangelands, and an urban site in Texas, USA. The effects of growth substrate, phytohormones, and salt treatments on seed germination were also evaluated to identify potential stimulus that can be used to manipulate germination in the species. Results of the study showed that silverleaf nightshade seeds from the agricultural farm were the largest, while those from the Littlefield rangeland were the smallest. Seeds collected from the urban site and agricultural farm have higher germination rates than those sampled from the rangelands. Compared to domesticated crops, silverleaf nightshade seeds require longer imbibition time. Seed germination was better in potting mix than in sand or combined potting mix and sand and was significantly reduced by salt and abscisic acid treatments. Overall, results of the study highlight the crucial role of local environments in conditioning the transgenerational adaptation of species, particularly with respect to germination. Recommendations for silverleaf nightshade control are presented based on the observed variations in the germination behavior of populations within specific ranges.

Intraspecific plasticity and trans-generational adaptation of reproductive traits and early development in a temperate marine neogastropod

Climate warming is altering the distribution of species, producing range shifts and promoting local extinctions. There is an urgent need to understand the underlying mechanisms that influence the persistence of populations across a species' distribution range in the face of global warming. Ocenebra erinaceus is a marine gastropod that exhibits high intraspecific variability in maternal investment and physiological capacity during early stages, which suggests local adaptation to natal environmental conditions. In this study, reproductive traits and trans-generational adaptation were measured in two subtidal populations: one from the middle (the Solent, UK) and another towards the southern end of their geographic distribution (Arcachon, France). Local adaptation was evaluated with a transfer experiment (i.e. Arcachon females transferred to Solent thermal conditions) and trans-generational adaptation was evaluated in the thermal tolerance response of embryos exposed to temperatures between 10 and 20 °C. This study shows that both populations have similar fitness; however, there are adaptive costs to live under their natal location, resulting in trade-offs between reproductive traits. Transferred females show lower reproductive output, which suggests that females are maladapted to live under a new environment. The trans-generational experiment demonstrates contrasting thermal tolerance ranges between populations. Adaptation to local thermal conditions was observed in transferred embryos, showing poor performance and high mortalities under the new environment. Our results provide a better understanding of intraspecific differences and adaptations across a species’ distribution range and provide insights into how climate warming will impact encapsulated species exhibiting location-specific adaptation.

Unconscious Collusions and Radioactive Identifications: When an Analyst’s Personal Experience of a Traumatized Society Meets a Patient’s Developmental Trauma

A case vignette of a woman with multiple developmental traumas is presented to illustrate the potential collusion of her self-protective retreats and powerful projections with the analyst’s own countertransference, which was colored by his transgenerational adaptation to a totalitarian political condition. The author, an analyst from the Czech Republic, explores his passive interpretative stance and extended capacity to tolerate the patient’s retreat and her fear of disclosing her true thoughts in light of “false adaptations” known in former Communist states. Psychoanalytic models of intrapsychic functioning of residents and psychoanalysts under the Communist regime are described. Finally, the author examines how his analytic functioning is impacted by his own ancestors’ adaptations, his own upbringing, and his own psychoanalytic training.

Paternal Age and Transgenerational Telomere Length Maintenance: A Simulation Model

Telomere length (TL) in offspring is positively correlated with paternal age at the time of the offspring conception. The paternal-age-at-conception (PAC) effect on TL is puzzling, and its biological implication at the population level is unknown. Using a probabilistic model of transgenerational TL and population dynamics, we simulated the effect of PAC on TL in individuals over the course of 1,000 years. Findings suggest a key role for an isometric PAC midpoint (PACmp) in modulating TL across generations, such that offspring conceived by males younger than the isometric PACmp have comparatively short telomeres, while offspring conceived by males older than the isometric PACmp have comparatively long telomeres. We further show that when cancer incidence escalates, the average PAC drops below the isometric PACmp and transgenerational adaptation to cancer ensues through TL shortening. We propose that PAC serves to maintain an optimal TL across generations.

Developmental carryover effects of ocean warming and acidification in corals from a potential climate refugium, the Gulf of Aqaba.

Coral reefs are degrading from the effects of anthropogenic activities, including climate change. Under these stressors, their ability to survive depends upon existing phenotypic plasticity, but also transgenerational adaptation. Parental effects are ubiquitous in nature, yet empirical studies of these effects in corals are scarce, particularly in the context of climate change. This study exposed mature colonies of the common reef-building coral Stylophora pistillata from the Gulf of Aqaba to seawater conditions likely to occur just beyond the end of this century during the peak planulae brooding season (Representative Concentration Pathway 8.5: pH -0.4 and +5°C beyond present day). Parent and planulae physiology were assessed at multiple time points during the experimental incubation. After 5weeks of incubation, the physiology of the parent colonies exhibited limited treatment-induced changes. All significant time-dependent changes in physiology occurred in both ambient and treatment conditions. Planulae were also resistant to future ocean conditions, with protein content, symbiont density, photochemistry, survival and settlement success not significantly different compared with under ambient conditions. High variability in offspring physiology was independent of parental or offspring treatments and indicate the use of a bet-hedging strategy in this population. This study thus demonstrates weak climate-change-associated carryover effects. Furthermore, planulae display temperature and pH resistance similar to those of adult colonies and therefore do not represent a larger future population size bottleneck. The findings add support to the emerging hypothesis that the Gulf of Aqaba may serve as a coral climate change refugium aided by these corals' inherent broad physiological resistance.

Cadmium-induced and trans-generational changes in the cultivable and total seed endophytic community of Arabidopsis thaliana.

Trans-generational adaptation is important to respond rapidly to environmental challenges and increase overall plant fitness. Besides well-known mechanisms such as epigenetic modifications, vertically transmitted endophytic bacteria might contribute to this process. The cultivable and total endophytic communities of several generations of Arabidopsis thaliana seeds harvested from plants exposed to cadmium (Cd) or not exposed were investigated. The diversity and richness of the seed endophytic community decreased with an increasing number of generations. Aeromicrobium and Pseudonocardia were identified as indicator species in seeds from Cd-exposed plants, while Rhizobium was abundantly present in both seed types. Remarkably, Rhizobium was the only genus that was consistently detected in seeds of all generations, which suggests that the phenotypic characteristics were more important as selection criteria for which bacteria are transferred to the next plant generation than the actual genera. Production of IAA was an important trait for endophytes from both seed types, while ACC deaminase activity and Cd tolerance were mainly associated with seed endophytes from Cd-exposed plants. Understanding how different factors influence the seed endophytic community can help us to improve seed quality and plant growth through different biotechnological applications.

MSH1 Is a Plant Organellar DNA Binding and Thylakoid Protein under Precise Spatial Regulation to Alter Development

As metabolic centers, plant organelles participate in maintenance, defense, and signaling. MSH1 is a plant-specific protein involved in organellar genome stability in mitochondria and plastids. Plastid depletion of MSH1 causes heritable, non-genetic changes in development and DNA methylation. We investigated the msh1 phenotype using hemi-complementation mutants and transgene-null segregants from RNAi suppression lines to sub-compartmentalize MSH1 effects. We show that MSH1 expression is spatially regulated, specifically localizing to plastids within the epidermis and vascular parenchyma. The protein binds DNA and localizes to plastid and mitochondrial nucleoids, but fractionation and protein–protein interactions data indicate that MSH1 also associates with the thylakoid membrane. Plastid MSH1 depletion results in variegation, abiotic stress tolerance, variable growth rate, and delayed maturity. Depletion from mitochondria results in 7%–10% of plants altered in leaf morphology, heat tolerance, and mitochondrial genome stability. MSH1 does not localize within the nucleus directly, but plastid depletion produces non-genetic changes in flowering time, maturation, and growth rate that are heritable independent of MSH1. MSH1 depletion alters non-photoactive redox behavior in plastids and a sub-set of mitochondrially altered lines. Ectopic expression produces deleterious effects, underlining its strict expression control. Unraveling the complexity of the MSH1 effect offers insight into triggers of plant-specific, transgenerational adaptation behaviors.

Transgenerational Adaptation to Pollution Changes Energy Allocation in Populations of Nematodes.

Assessing the evolutionary responses of long-term exposed populations requires multigeneration ecotoxicity tests. However, the analysis of the data from these tests is not straightforward. Mechanistic models allow the in-depth analysis of the variation of physiological traits over many generations, by quantifying the trend of the physiological and toxicological parameters of the model. In the present study, a bioenergetic mechanistic model has been used to assess the evolution of two populations of the nematode Caenorhabditis elegans in control conditions or exposed to uranium. This evolutionary pressure resulted in a brood size reduction of 60%. We showed an adaptation of individuals of both populations to experimental conditions (increase of maximal length, decrease of growth rate, decrease of brood size, and decrease of the elimination rate). In addition, differential evolution was also highlighted between the two populations once the maternal effects had been diminished after several generations. Thus, individuals that were greater in maximal length, but with apparently a greater sensitivity to uranium were selected in the uranium population. In this study, we showed that this bioenergetics mechanistic modeling approach provided a precise, certain, and powerful analysis of the life strategy of C. elegans populations exposed to heavy metals resulting in an evolutionary pressure across successive generations.

Relationship between trans-generational effects of tetracycline on Daphnia magna at the physiological and whole organism level

The effects of pharmaceuticals have been underestimated during single generation exposure. Therefore, in this study, we investigated toxic responses at the physiological and whole organism level in tetracycline-exposed Daphnia magna over four consecutive generational lifecycles. The results showed that tetracycline affected energy-related physiological functions in concentration- and generation-dependent manners, and especially maintenance costs increased. Consequently, multigenerational exposure to tetracycline induced changes in energy balance, resulting in the change of higher levels of biological responses. In contrast, D. magna acclimated to tetracycline exposure over multiple generations, as evidenced by the increased LC50 values. Transgenerational adaptation was related to the neonatal sensitivity and energy reserves of the organism. The results also emphasized the idea that the number of generation is an important factor for toxicity. The present study confirmed that toxic stress induces metabolic changes in an organism, thereby leading to increased energy consumption that results in adverse effects on reproduction.

Transgenerational adaptation to heavy metal salts in Arabidopsis

Exposure to abiotic and biotic stress results in changes in plant physiology and triggers genomic instability. Recent reports suggest that the progeny of stressed plants also exhibit changes in genome stability, stress tolerance, and methylation. Here we analyzed whether exposure to Ni2+, Cd2+, and Cu2+ salts leads to transgenerational changes in homologous recombination frequency and stress tolerance. We found that the immediate progeny of stressed plants exhibited an increased rate of recombination. However, when the progeny of stressed plants was propagated without stress, recombination reverted to normal levels. Exposure of plants to heavy metals for five consecutive generations (S1–S5) resulted in recombination frequency being maintained at a high level. Skipping stress following two to three generations of propagation with 50 mM Ni2+ or Cd2+ did not decrease the recombination frequency, suggesting plant acclimation to upregulated recombination. Analysis of the progeny of plants exposed to Cu2+ and Ni2+ indicated higher stress tolerance to the heavy metal parental plants were exposed to. Tolerance was higher in plants propagated with stress for three to five generations, which resulted in longer roots than plants propagated on heavy metals for only one to two generations. Tolerance was also more prominent upon exposure to a higher concentration of salts. The progeny of stressed plants were also more tolerant to NaCl and methyl methane sulfonate.

Male-line transgenerational responses in humans

Genomic imprinting establishes the principle of epigenetic marks placed in one generation influencing gene expression in the next generation. This led to speculation that epigenetic gametic inheritance might underlie a form of transgenerational adaptation to major environmental challenges, such that exposures in one generation correlate with outcomes in the next generation(s). An ongoing collaboration between Umeå University, Sweden and the Avon Longitudinal Study of Parents and Childhood, Bristol University, UK has documented transgenerational correlations between food supply during the early life of the paternal grandparents and the grandchild's longevity, including associations with cardiovascular and diabetic deaths, and correlations between the onset of paternal smoking in mid-childhood and the body mass index of future sons. Whilst the mediating molecular mechanism(s) is unknown, the sex-specific transmission patterns and exposure-sensitive periods suggest a pre-evolved transgenerational response mechanism.

Correction: Transgenerational Adaptation of Arabidopsis to Stress Requires DNA Methylation and the Function of Dicer-Like Proteins

Correction: Transgenerational Adaptation of Arabidopsis to Stress Requires DNA Methylation and the Function of Dicer-Like Proteins