Cultural and genetic inheritance combine to enable rapid changes in trait expression, but their relative importance in determining trait expression across generations is not clear. Birdsong is a socially learned cognitive trait that is subject to both cultural and genetic inheritance, as well as being affected by early developmental conditions. We sought to test whether early-life conditions in one generation can affect song acquisition in the next generation. We exposed one generation (F1) of nestlings to elevated corticosterone (CORT) levels, allowed them to breed freely as adults, and quantified their son\'s (F2) ability to copy the song of their social father. We also quantified the neurogenetic response to song playback through immediate early gene (IEG) expression in the auditory forebrain. F2 males with only one corticosterone-treated parent copied their social father\'s song less accurately than males with two control parents. Expression of ARC in caudomedial nidopallium (NCM) correlated with father-son song similarity, and patterns of expression levels of several IEGs in caudomedial mesopallium (CMM) in response to father song playback differed between control F2 sons and those with a CORT-treated father only. This is the first study to demonstrate that developmental conditions can affect social learning and neurogenetic responses in a subsequent generation.

UNASSIGNED: Warming generally induces faster developmental and growth rates, resulting in smaller asymptotic sizes of adults in warmer environments (a pattern known as the temperature-size rule). However, whether temperature-size responses are affected across generations, especially when thermal environments differ from one generation to the next, is unclear. Here, we tested temperature-size responses at different ontogenetic stages and in two consecutive generations using two soil-living Collembola species from the family Isotomidae: Folsomia candida (asexual) and Proisotoma minuta (sexually reproducing).
UNASSIGNED: We used individuals (progenitors; F0) from cultures maintained during several generations at 15 °C or 20 °C, and exposed their offspring in cohorts (F1) to various thermal environments (15 °C, 20 °C, 25 °C and 30 °C) during their ontogenetic development (from egg laying to first reproduction; i.e., maturity). We measured development and size traits in the cohorts (egg diameter and body length at maturity), as well as the egg diameters of their progeny (F2). We predicted that temperature-size responses would be predominantly determined by within-generation plasticity, given the quick responsiveness of growth and developmental rates to changing thermal environments. However, we also expected that mismatches in thermal environments across generations would constrain temperature-size responses in offspring, possibly due to transgenerational plasticity.
UNASSIGNED: We found that temperature-size responses were generally weak in the two Collembola species, both for within- and transgenerational plasticity. However, egg and juvenile development were especially responsive at higher temperatures and were slightly affected by transgenerational plasticity. Interestingly, plastic responses among traits varied non-consistently in both Collembola species, with some traits showing plastic responses in one species but not in the other and vice versa. Therefore, our results do not support the view that the mode of reproduction can be used to explain the degree of phenotypic plasticity at the species level, at least between the two Collembola species used in our study. Our findings provide evidence for a general reset of temperature-size responses at the start of each generation and highlight the importance of measuring multiple traits across ontogenetic stages to fully understand species\' thermal responses.

Population and species persistence in a rapidly warming world will be determined by an organism\'s ability to acclimate to warmer conditions, especially across generations. There is potential for transgenerational acclimation but the importance of ontogenetic timing in the transmission of environmentally induced parental effects remains mostly unknown. We aimed to disentangle the effects of two critical ontogenetic stages (juvenile development and reproduction) to the new-generation acclimation potential, by exposing the spiny chromis damselfish Acanthochromis polyacanthus to simulated ocean warming across two generations. By using hepatic transcriptomics, we discovered that the post-hatching developmental environment of the offspring themselves had little effect on their acclimation potential at 2.5 months of life. Instead, the developmental experience of parents increased regulatory RNA production and protein synthesis, which could improve the offspring\'s response to warming. Conversely, parental reproduction and offspring embryogenesis in warmer water elicited stress response mechanisms in the offspring, with suppression of translation and mitochondrial respiration. Mismatches between parental developmental and reproductive temperatures deeply affected offspring gene expression profiles, and detrimental effects were evident when warming occurred both during parents\' development and reproduction. This study reveals that the previous generation\'s developmental temperature contributes substantially to thermal acclimation potential during early life; however, exposure at reproduction as well as prolonged heat stress will likely have adverse effects on the species\' persistence.

The effect of UV-B radiation exposure on transgenerational plasticity, the phenomenon whereby the parental environment influences both the parent\'s and the offspring\'s phenotype, is poorly understood. To investigate the impact of exposing successive generations of rice plants to UV-B radiation on seed morphology and proanthocyanidin content, the local traditional rice variety \'Baijiaolaojing\' was planted on terraces in Yuanyang county and subjected to enhanced UV-B radiation treatments. The radiation intensity that caused the maximum phenotypic plasticity (7.5 kJ·m-2) was selected for further study, and the rice crops were cultivated for four successive generations. The results show that in the same generation, enhanced UV-B radiation resulted in significant decreases in grain length, grain width, spike weight, and thousand-grain weight, as well as significant increases in empty grain percentage and proanthocyanidin content, compared with crops grown under natural light conditions. Proanthocyanidin content increased as the number of generations of rice exposed to radiation increased, but in generation G3, it decreased, along with the empty grain ratio. At the same time, biomass, tiller number, and thousand-grain weight increased, and rice growth returned to control levels. When the offspring\'s radiation memory and growth environment did not match, rice growth was negatively affected, and seed proanthocyanidin content was increased to maintain seed activity. The correlation analysis results show that phenylalanine ammonialyase (PAL), cinnamate-4-hydroxylase (C4H), dihydroflavonol 4-reductase (DFR), and 4-coumarate:CoA ligase (4CL) enzyme activity positively influenced proanthocyanidin content. Overall, UV-B radiation affected transgenerational plasticity in seed morphology and proanthocyanidin content, showing that rice was able to adapt to this stressor if previous generations had been continuously exposed to treatment.

The environment experienced by one generation has the potential to affect the subsequent one through non-genetic inheritance of parental effects. Since both mothers and fathers can influence their offspring, questions arise regarding how the maternal, paternal and offspring experiences integrate into the resulting phenotype. We aimed to disentangle the maternal and paternal contributions to transgenerational thermal acclimation in a reef fish, Acanthochromis polyacanthus, by exposing two generations to elevated temperature (+1.5°C) in a fully factorial design and analysing the F2 hepatic gene expression. Paternal and maternal effects showed not only common but also parent-specific components, with the father having the largest influence in shaping the offspring\'s transcriptomic profile. Fathers contributed to transcriptional transgenerational response to warming through transfer of epigenetically controlled stress-response mechanisms while mothers influenced increased gene expression associated with lipid metabolism regulation. However, the key to acclimation potential was matching thermal experiences of the parents. When both parents were exposed to the same condition, offspring showed increased expression of genes related to structural RNA production and transcriptional regulation, whereas environmental mismatch in parents resulted in maladaptive parental condition transfer, revealed by translation suppression and endoplasmic reticulum stress. Interestingly, the offspring\'s own environmental experience had the smallest influence on their hepatic transcription profiles. Taken together, our results show the complex nature of the interplay among paternal, maternal and offspring cue integration, and reveal that acclimation potential to ocean warming might depend not only on maternal and paternal contributions but importantly on congruent parental thermal experiences.

OBJECTIVE: Intra- and transgenerational plasticity may provide substantial phenotypic variation to cope with environmental change. Since assessing the unique contribution of the maternal environment to the offspring phenotype is challenging in perennial, outcrossing plants, little is known about the evolutionary and ecological implications of transgenerational plasticity and its persistence over the life cycle in these species. We evaluated how intra- and transgenerational plasticity interplay to shape the adaptive responses to drought in two perennial Mediterranean shrubs.
METHODS: We used a novel common garden approach that reduced within-family genetic variation in both the maternal and offspring generations by growing the same maternal individual in two contrasting watering environments, well-watered and drought, in consecutive years. We then assessed phenotypic differences at the reproductive stage between offspring reciprocally grown in the same environments.
RESULTS: Maternal drought had an effect on offspring performance only in Helianthemum squamatum. Offspring of drought-stressed plants showed more inflorescences, less sclerophyllous leaves and higher growth rates in both watering conditions, and heavier seeds under drought, than offspring of well-watered maternal plants. Maternal drought also induced similar plasticity patterns across maternal families, showing a general increase in seed mass in response to offspring drought, a pattern not observed in the offspring of well-watered plants. In contrast, both species expressed immediate adaptive plasticity, and the magnitude of intragenerational plasticity was larger than the transgenerational plastic responses.
CONCLUSIONS: Our results highlight that adaptive effects associated with maternal drought can persist beyond the seedling stage and provide evidence of species-level variation in the expression of transgenerational plasticity. Such differences between co-occurring Mediterranean species in the prevalence of this form of non-genetic inheritance may result in differential vulnerability to climate change.

It has long been recognized that the environment experienced by parents can influence the traits of offspring (i.e. \'parental effects\'). Much research has explored whether mothers respond to predictable shifts in environmental signals by modifying offspring phenotypes to best match future conditions. Many organisms experience conditions that theory predicts should favor the evolution of such \'anticipatory parental effects\', but such predictions have received limited empirical support. \'Condition transfer effects\' are an alternative to anticipatory effects that occur when the environment experienced by parents during development influences offspring fitness. Condition transfer effects occur when parents that experience high-quality conditions produce offspring that exhibit higher fitness irrespective of the environmental conditions in the offspring generation. Condition transfer effects are not driven by external signals but are instead a byproduct of past environmental quality. They are also likely adaptive but have received far less attention than anticipatory effects. Here, we review the generality of condition transfer effects and show that they are much more widespread than is currently appreciated. Condition transfer effects are observed across taxa and are commonly associated with experimental manipulations of resource conditions experienced by parents. Our Review calls for increased research into condition transfer effects when considering the role of parental effects in ecology and evolution.

BACKGROUND: Despite the increasing number of epigenomic studies in plants, little is known about the forces that shape the methylome in long-lived woody perennials. The Lombardy poplar offers an ideal opportunity to investigate the impact of the individual environmental history of trees on the methylome.
RESULTS: We present the results of three interconnected experiments on Lombardy poplar. In the first experiment, we investigated methylome variability during a growing season and across vegetatively reproduced generations. We found that ramets collected over Europe and raised in common conditions have stable methylomes in symmetrical CG-contexts. In contrast, seasonal dynamics occurred in methylation patterns in CHH context. In the second experiment, we investigated whether methylome patterns of plants grown in a non-parental environment correlate with the parental climate. We did not observe a biological relevant pattern that significantly correlates with the parental climate. Finally, we investigated whether the parental environment has persistent carry-over effects on the vegetative offspring\'s phenotype. We combined new bud set observations of three consecutive growing seasons with former published bud set data. Using a linear mixed effects analysis, we found a statistically significant but weak short-term, parental carry-over effect on the timing of bud set. However, this effect was negligible compared to the direct effects of the offspring environment.
CONCLUSIONS: Genome-wide cytosine methylation patterns in symmetrical CG-context are stable in Lombardy poplar and appear to be mainly the result of random processes. In this widespread poplar clone, methylation patterns in CG-context can be used as biomarkers to infer a common ancestor and thus to investigate the recent environmental history of a specific Lombardy poplar. The Lombardy poplar shows high phenotypic plasticity in a novel environment which enabled this clonal tree to adapt and survive all over the temperate regions of the world.

Dormancy represents an investment with its own costs and benefit. Besides the advantage obtained from the avoidance of harsh environments and from the synchronization of life cycles with seasonal changes, an organism could benefit from a temporary stop in growth and reproduction. To test this hypothesis a transgenerational experiment was carried out comparing the life history traits of clonal females of Eucypris virens from resting and non-resting eggs at two different photoperiods: short day length (6:18 L:D), proxy of favorable but unpredictable late winter-spring hydroperiod, and long day length (16:8 L:D) proxy of dry predictable unfavorable season, inducing resting egg production and within-generation plasticity (WGP). Clonal females that were dormancy deprived showed the highest age at first deposition and the lowest fecundity. Dormancy seems to work as a resetting mechanism of reproduction. Transgenerational plasticity (TGP) had a bounce back pattern: the phenotype of F1 generation was influenced by cues experienced in the F0 generation but the effects of F0 exposure were not evident in the F2. TGP might be adaptive when a mother experiences some kind of seasonality or stochasticity producing both resting and nonresting eggs. A positive relationship between the number of resting eggs and the total number of eggs per females suggested the absence of trade-off between dormancy and reproduction. Both WGP and TGP increase the mother long term fitness with important consequences on population dynamics, on the way a species spread throughout space and time and might respond to climate change.

Parental care is a critical determinant of offspring fitness, and parents adjust their care in response to ecological challenges, including predation risk. The experiences of both mothers and fathers can influence phenotypes of future generations (transgenerational plasticity). If it is adaptive for parents to alter parental care in response to predation risk, then we expect F1 and F2 offspring who receive transgenerational cues of predation risk to shift their parental care behaviour if these ancestral cues reliably predict a similarly risky environment as their F0 parents. Here, we used three-spined sticklebacks (Gasterosteus aculeatus) to understand how paternal exposure to predation risk prior to mating alters reproductive traits and parental care behaviour in unexposed F1 sons and F2 grandsons. Sons of predator-exposed fathers took more attempts to mate than sons of control fathers. F1 sons and F2 grandsons with two (maternal and paternal) predator-exposed grandfathers shifted their paternal care (fanning) behaviour in strikingly similar ways: they fanned less initially, but fanned more near egg hatching. This shift in fanning behaviour matches shifts observed in response to direct exposure to predation risk, suggesting a highly conserved response to pre-fertilization predator exposure that persists from the F0 to the F1 and F2 generations.