Small-scale vegetation patterns in the parental environment influence the phase state of hatchlings of the desert locust

Desert locusts (Schistocerca gregaria Forskål (Orthoptera: Acrididae)) change phase in response to population density. Solitarious insects avoid one another; when crowded, they shift to the gregarious phase and aggregate. Laboratory experiments and individual‐based modelling have shown that small‐scale resource distribution can affect locust phase state via an influence on crowding. Laboratory work has also shown that parental phase state is transmitted to offspring via maternal inheritance. These effects had not been investigated in the field previously. We maintained small populations of adult desert locusts in semi‐field enclosures with different distribution patterns of a single plant species (Hyoscyamus muticus L. (Solanaceae)). The offspring of locusts exposed to more clumped patterns of vegetation exhibited more gregarious behaviour when tested in a behavioural phase assay than did progeny from parents left in enclosures with more scattered vegetation. These effects on nymphal behaviour appeared to be mediated by influences of resource distribution on adult phase state. Phase state in small semi‐field populations was influenced by small‐scale vegetation distribution. Phase differences engendered by environmental structure were maintained in time and transmitted to progeny.     

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.     

Paternal high-fat diet alters triglyceride metabolism-related gene expression in liver and white adipose tissue of male mouse offspring

Obesity is a major public health problem, and its prevalence is progressively increasing worldwide. In addition, accumulating evidence suggests that diverse nutritional and metabolic disturbances including obesity can be transmitted from parents to offspring via transgenerational epigenetic inheritance. The previous reports have shown that paternal obesity has profound impacts on the development and metabolic health of their progeny. However, little information is available concerning the effects of paternal high-fat diet (HFD) exposure on triglyceride metabolism in the offspring. Therefore, we investigated the effects of paternal HFD on triglyceride metabolism and related gene expression in male mouse offspring. We found that paternal HFD exposure significantly increased the body weight, liver and epididymal white adipose tissue (eWAT) weights, and liver triglyceride content in male offspring, despite consuming control diet. In addition, paternal HFD exposure had induced changes in the mRNA expression of genes involved in lipid and triglyceride metabolism in the liver and eWAT. These findings indicate transgenerational inheritance from the paternal metabolic disturbance of triglyceride and support the effects of paternal lifestyle choices on offspring development and health later in life.     

Parent‐of‐origin control of transgenerational retrotransposon proliferation in Arabidopsis

Retrotransposons are ubiquitous mobile genetic elements constituting a major part of eukaryotic genomes. Yet, monitoring retrotransposition and subsequent copy number increases in multicellular eukaryotes is intrinsically difficult. By following the transgenerational accumulation of a newly activated retrotransposon EVADE (EVD) in Arabidopsis, we noticed fast expansion of activated elements transmitted through the paternal germ line but suppression when EVD‐active copies are maternally inherited. This parent‐of‐origin effect on EVD proliferation was still observed when gametophytes carried mutations for key epigenetic regulators previously shown to restrict EVD mobility. Therefore, the main mechanism preventing active EVD proliferation seems to act through epigenetic control in sporophytic tissues in the mother plant. In consequence, once activated, this retrotransposon proliferates in plant populations owing to suppressed epigenetic control during paternal transmission. This parental gateway might contribute to the occasional bursts of retrotransposon mobilization deduced from the genome sequences of many plant species.     

Epigenetics and the origins of paternal effects

Though there are multiple routes through which parents can influence their offspring, recent studies of environmentally induced epigenetic variation have highlighted the role of non-genomic pathways. In addition to the experience-dependent modification of DNA methylation that can be achieved via mother-infant interactions, there has been increasing interest in the epigenetic mechanisms through which paternal influences on offspring development can be achieved. Epidemiological and laboratory studies suggest that paternal nutritional and toxicological exposures as well as paternal age and phenotypic variation can lead to variations in offspring and, in some cases, grand-offspring development. These findings suggest a potential epigenetic germline inheritance of paternal effects. However, it may be important to consider the interplay between maternal and paternal influences as well as the experimental dissociation between experience-dependent and germline transmission when exploring the role of epigenetic variation within the germline as a mediator of these effects. In this review, we will explore these issues, with a particular focus on the potential role of paternally induced maternal investment, highlight the literature illustrating the transgenerational impact of paternal experiences, and discuss the evidence supporting the role of epigenetic mechanisms in maintaining paternal effects both within and across generations.     

How differing modes of non‐genetic inheritance affect population viability in fluctuating environments

Different modes of non‐genetic inheritance are expected to affect population persistence in fluctuating environments. We here analyse Caenorhabditis elegans density‐independent per capita growth rate time series on 36 populations experiencing six controlled sequences of challenging oxygen level fluctuations across 60 generations, and parameterise competing models of non‐genetic inheritance in order to explain observed dynamics. Our analysis shows that phenotypic plasticity and anticipatory maternal effects are sufficient to explain growth rate dynamics, but that a carryover model where ‘epigenetic’ memory is imperfectly transmitted and might be reset at each generation is a better fit to the data. We further find that this epigenetic memory is asymmetric since it is kept for longer when populations are exposed to the more challenging environment. Our analysis suggests that population persistence in fluctuating environments depends on the non‐genetic inheritance of phenotypes whose expression is regulated across multiple generations.     

Long-term and transgenerational effects of in vitro culture on mouse embryos

The mouse is a convenient model to analyze the impact of in vitro culture (IVC) on the long-term health and physiology of the offspring, and the possible inheritance of these altered phenotypes. The preimplantation period of mammalian development has been identified as an early ‘developmental window’ during which environmental conditions may influence the pattern of future growth and physiology. Suboptimal culture media can cause severe alterations in mRNA expression in the embryo, which are associated with embryo quality reduction. In addition, the embryonic epigenetic reprogramming may also be severely affected by IVC, modifying epigenetic marks particularly in imprinted genes and epigenetically sensitive alleles. These altered epigenetic marks can persist after birth, resulting in adult health problems such as obesity, increased anxiety and memory deficits. Furthermore, some epigenetic modifications have been found to be transmitted to the offspring (epigenetic transgenerational inheritance), thereby providing a suitable model to asses risks of cross-generational effects of perturbing early embryo development. This review will highlight how preimplantation environment changes can not only affect developmental processes taking place at that time, but can also have an impact further, affecting offspring health and physiology; and how they may be transmitted to the next generation. We will also analyze the emerging role of epigenetics as a mechanistic link between the early environment and the later phenotype of the developing organism.     

Three epigenetic information channels and their different roles in evolution

There is increasing evidence for epigenetically mediated transgenerational inheritance across taxa. However, the evolutionary implications of such alternative mechanisms of inheritance remain unclear. Herein, we show that epigenetic mechanisms can serve two fundamentally different functions in transgenerational inheritance: (i) selection-based effects, which carry adaptive information in virtue of selection over many generations of reliable transmission; and (ii) detection-based effects, which are a transgenerational form of adaptive phenotypic plasticity. The two functions interact differently with a third form of epigenetic information transmission, namely information about cell state transmitted for somatic cell heredity in multicellular organisms. Selection-based epigenetic information is more likely to conflict with somatic cell inheritance than is detection-based epigenetic information. Consequently, the evolutionary implications of epigenetic mechanisms are different for unicellular and multicellular organisms, which underscores the conceptual and empirical importance of distinguishing between these two different forms of transgenerational epigenetic effect.     

The Information Value of Non-Genetic Inheritance in Plants and Animals

Parents influence the development of their offspring in many ways beyond the transmission of DNA. This includes transfer of epigenetic states, nutrients, antibodies and hormones, and behavioural interactions after birth. While the evolutionary consequences of such non-genetic inheritance are increasingly well understood, less is known about how inheritance mechanisms evolve. Here, we present a simple but versatile model to explore the adaptive evolution of non-genetic inheritance. Our model is based on a switch mechanism that produces alternative phenotypes in response to different inputs, including genes and non-genetic factors transmitted from parents and the environment experienced during development. This framework shows how genetic and non-genetic inheritance mechanisms and environmental conditions can act as cues by carrying correlational information about future selective conditions. Differential use of these cues is manifested as different degrees of genetic, parental or environmental morph determination. We use this framework to evaluate the conditions favouring non-genetic inheritance, as opposed to genetic determination of phenotype or within-generation plasticity, by applying it to two putative examples of adaptive non-genetic inheritance: maternal effects on seed germination in plants and transgenerational phase shift in desert locusts. Our simulation models show how the adaptive value of non-genetic inheritance depends on its mechanism, the pace of environmental change, and life history characteristics.     

Transduction of high‐density signals across generations in aphid wing polyphenism

Wing polyphenism in aphids represents an outstanding example of adaptive phenotypic plasticity. During summer, parthenogenic mother aphids alter the developmental fate of their embryos to produce wingless or winged adult forms in response to high population density (i.e. crowded conditions). Although this maternal effect is well known, the mechanisms underlying transgenerational winged‐morph determination remain largely unresolved. In the present study, the effects of different high‐density treatment durations are tested on the vetch aphid Megoura crassicauda Mordvilko aiming to investigate how and when the density signals detected by mothers are transmitted to embryos. The duration of density treatment shows additive effects on both the number of crowded females producing winged aphids (winged‐producers) and the number of winged progeny. In addition, even when high‐density treatment is stopped, the production of winged offspring continues for several days and depends on the duration of treatment. The results indicate that mother aphids retain high‐density signals for a period after removal of the stimulus. Furthermore, observations of the progeny sequence (i.e. the order in which the offspring are born) and the embryonic stages developing in the mothers reveal that high‐density information may affect embryonic fate at the late embryonic stage immediately before cuticle formation.     

A paternal environmental legacy: Evidence for epigenetic inheritance through the male germ line

Literature on maternal exposures and the risk of epigenetic changes or diseases in the offspring is growing. Paternal contributions are often not considered. However, some animal and epidemiologic studies on various contaminants, nutrition, and lifestyle‐related conditions suggest a paternal influence on the offspring's future health. The phenotypic outcomes may have been attributed to DNA damage or mutations, but increasing evidence shows that the inheritance of environmentally induced functional changes of the genome, and related disorders, are (also) driven by epigenetic components. In this essay we suggest the existence of epigenetic windows of susceptibility to environmental insults during sperm development. Changes in DNA methylation, histone modification, and non‐coding RNAs are viable mechanistic candidates for a non‐genetic transfer of paternal environmental information, from maturing germ cell to zygote. Inclusion of paternal factors in future research will ultimately improve the understanding of transgenerational epigenetic plasticity and health‐related effects in future generations.     

Syntaxin 1A modulates the sexual maturity rate and progeny egg size related to phase changes in locusts

The migratory locust (Locusta migratoria) exhibits clear phenotypic plasticity depending on its population density. Previous studies have explored the molecular mechanisms of body colour, behavior, immunity, and metabolism between high population density gregarious (G) and low population density solitarious (S) locusts. However, the molecular mechanisms underlying differences in reproductive traits remain unknown. G locusts reach sexual maturation much faster and lay larger eggs compared with S locusts. The traits of G locusts decreased significantly with isolation, whereas those of S locusts increased with crowding. Analysis of gene expression in female adults indicated that syntaxin 1A (Syx1A) was expressed significantly higher in G locusts than in S locusts. After silencing Syx1A expression in G locusts by RNA interference (RNAi), their sexual maturity rate and progeny egg size changed towards those of S locusts. Similarly, increment in the traits of S locusts with crowding was blocked by Syx1A interference. Changes in the traits were also confirmed by decrease in the level of vitellogenin, which is regulated by Syx1A. In conclusion, plasticity of the sexual maturity rate and progeny egg size of G and S locusts, which is beneficial for locusts to adapt to environmental changes, is regulated by Syx1A.     

Increased transgenerational epigenetic variation,but not predictable epigenetic variants,after environmental exposure in two apomictic dandelion lineages

DNA methylation is one of the mechanisms underlying epigenetic modifications. DNA methylations can be environmentally induced and such induced modifications can at times be transmitted to successive generations. However, it remains speculative how common such environmentally induced transgenerational DNA methylation changes are and if they persist for more than one offspring generation. We exposed multiple accessions of two different apomictic dandelion lineages of the Taraxacum officinale group (Taraxacum alatum and T. hemicyclum) to drought and salicylic acid (SA) treatment. Using methylation‐sensitive amplified fragment length polymorphism markers (MS‐AFLPs) we screened anonymous methylation changes at CCGG restriction sites throughout the genome after stress treatments and assessed the heritability of induced changes for two subsequent unexposed offspring generations. Irrespective of the initial stress treatment, a clear buildup of heritable DNA methylation variation was observed across three generations, indicating a considerable background rate of heritable epimutations. Less evidence was detected for environmental effects. Drought stress showed some evidence for accession‐specific methylation changes, but only in the exposed generation and not in their offspring. By contrast, SA treatment caused an increased rate of methylation change in offspring of treated plants. These changes were seemingly undirected resulting in increased transgenerational epigenetic variation between offspring individuals, but not in predictable epigenetic variants. While the functional consequences of these MS‐AFLP‐detected DNA methylation changes remain to be demonstrated, our study shows that (1) stress‐induced transgenerational DNA methylation modification in dandelions is genotype and context‐specific; and (2) inherited environmental DNA methylation effects are mostly undirected and not targeted to specific loci.     

Bacteria‐type‐specific biparental immune priming in the pipefish Syngnathus typhle

The transfer of acquired and specific immunity against previously encountered bacteria from mothers to offspring boosts the immune response of the next generation and supports the development of a successful pathogen defense. While most studies claim that the transfer of immunity is a maternal trait, in the sex‐role‐reversed pipefish Syngnathus typhle, fathers nurse the embryos over a placenta‐like structure, which opens the door for additional paternal immune priming. We examined the potential and persistence of bacteria‐type‐specific parental immune priming in the pipefish S. typhle over maturation time using a fully reciprocal design with two different bacteria species (Vibrio spp. and Tenacibaculum maritimum). Our results suggest that S. typhle is able to specifically prime the next generation against prevalent local bacteria and to a limited extent even also against newly introduced bacteria species. Long‐term protection was thereby maintained only against prevailing Vibrio bacteria. Maternal and paternal transgenerational immune priming can complement each other, as they affect different pathways of the offspring immune system and come with distinct degree of specificity. The differential regulation of DNA‐methylation genes upon parental bacteria exposure in premature pipefish offspring indicates that epigenetic regulation processes are involved in transferring immune‐related information across generations. The identified trade‐offs between immune priming and reproduction determine TGIP as a costly trait, which might constrain the evolution of long‐lasting TGIP, if parental and offspring generations do not share the same parasite assembly.     

Genetic variation for parental effects on the propensity to gregarise in <Emphasis Type="Italic">Locusta migratoria</Emphasis>

Background  

Environmental parental effects can have important ecological and evolutionary consequences, yet little is known about genetic variation among populations in the plastic responses of offspring phenotypes to parental environmental conditions. This type of variation may lead to rapid phenotypic divergence among populations and facilitate speciation. With respect to density-dependent phenotypic plasticity, locust species (Orthoptera: family Acrididae), exhibit spectacular developmental and behavioural shifts in response to population density, called phase change. Given the significance of phase change in locust outbreaks and control, its triggering processes have been widely investigated. Whereas crowding within the lifetime of both offspring and parents has emerged as a primary causal factor of phase change, less is known about intraspecific genetic variation in the expression of phase change, and in particular in response to the parental environment. We conducted a laboratory experiment that explicitly controlled for the environmental effects of parental rearing density. This design enabled us to compare the parental effects on offspring expression of phase-related traits between two naturally-occurring, genetically distinct populations of Locusta migratoria that differed in their historical patterns of high population density outbreak events.     

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.     

Epigenetic population differentiation in field‐ and common garden‐grown Scabiosa columbaria plants

Populations often differ in phenotype and these differences can be caused by adaptation by natural selection, random neutral processes, and environmental responses. The most straightforward way to divide mechanisms that influence phenotypic variation is heritable variation and environmental‐induced variation (e.g., plasticity). While genetic variation is responsible for most heritable phenotypic variation, part of this is also caused by nongenetic inheritance. Epigenetic processes may be one of the underlying mechanisms of plasticity and nongenetic inheritance and can therefore possibly contribute to heritable differences through drift and selection. Epigenetic variation may be influenced directly by the environment, and part of this variation can be transmitted to next generations. Field screenings combined with common garden experiments will add valuable insights into epigenetic differentiation, epigenetic memory and can help to reveal part of the relative importance of epigenetics in explaining trait variation. We explored both genetic and epigenetic diversity, structure and differentiation in the field and a common garden for five British and five French Scabiosa columbaria populations. Genetic and epigenetic variation was subsequently correlated with trait variation. Populations showed significant epigenetic differentiation between populations and countries in the field, but also when grown in a common garden. By comparing the epigenetic variation between field and common garden‐grown plants, we showed that a considerable part of the epigenetic memory differed from the field‐grown plants and was presumably environmentally induced. The memory component can consist of heritable variation in methylation that is not sensitive to environments and possibly genetically based, or environmentally induced variation that is heritable, or a combination of both. Additionally, random epimutations might be responsible for some differences as well. By comparing epigenetic variation in both the field and common environment, our study provides useful insight into the environmental and genetic components of epigenetic variation.     

Daphnia magna microRNAs respond to nutritional stress and ageing but are not transgenerational

Maternal effects, where the performance of offspring is determined by the condition of their mother, are widespread and may in some cases be adaptive. The crustacean Daphnia magna shows strong maternal effects: offspring size at birth and other proxies for fitness are altered when their mothers are older or when mothers have experienced dietary restriction. The mechanisms for this transgenerational transmission of maternal experience are unknown, but could include changes in epigenetic patterning. MicroRNAs (miRNAs) are regulators of gene expression that have been shown to play roles in intergenerational information transfer, and here, we test whether miRNAs are involved in D. magna maternal effects. We found that miRNAs were differentially expressed in mothers of different ages or nutritional state. We then examined miRNA expression in their eggs, their adult daughters and great granddaughters, which did not experience any treatments. The maternal (treatment) generation exhibited differential expression of miRNAs, as did their eggs, but this was reduced in adult daughters and lost by great granddaughters. Thus, miRNAs are a component of maternal provisioning, but do not appear to be the cause of transgenerational responses under these experimental conditions. MicroRNAs may act in tandem with egg provisioning (e.g., with carbohydrates or fats), and possibly other small RNAs or epigenetic modifications.