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1. Transgenerational phenotypic plasticity is increasingly recognized as an important buffer of environmental change – many studies show that mothers alter the phenotype of their offspring so as to maximize their performance in their local environment. Fewer studies have examined the capacity of parents to alter the phenotype of their gametes to cope with environmental change. In organisms that shed their gametes externally, gametes are extremely vulnerable to local stresses and transgenerational plasticity in the phenotypes of gametes seems likely in this group. 2. In a marine tubeworm, Hydroides diramphus, we manipulated the salinity environment that mothers and fathers experienced before reproduction and then examined the phenotype of their gametes, as well as the performance of those gametes and the resultant larvae in different salinities. 3. We found strong evidence for gamete plasticity – both mothers and fathers adaptively adjust the phenotype of their gametes to maximize the performance of those gametes in the salinity regime experienced by their parents. Parents were quite flexible in the phenotype of gametes that they produced: they could switch the salinity tolerance of their gametes back and forth depending on their most recent experience. 4. Gamete plasticity was not without risks, however. We observed strong trade-offs in performance when gametes experienced an environment that did not match that of their parents. These effects of the parental environment persist for the duration of the larval phase such that larvae may not be able to disperse to environments that do not match their parents. Gamete plasticity may therefore represent an important source of phenotype–environment mismatches. 5. Gamete plasticity may represent an important mechanism for coping with environmental change and an important source of maternal and paternal effects in species with external fertilization. Studies that seek to predict the impacts of stresses that persist across generations (e.g. ocean acidification) should include parental exposures to the stress of interest.

Social environment profoundly influences the fitness of animals, affecting their probability of survival to adulthood, longevity, and reproductive output. The social conditions experienced by parents at the time of reproduction can predict the social environments that offspring will face. Despite clear challenges in predicting future environmental conditions, adaptive maternal effects provide a mechanism of passing environmental information from parent to offspring and are now considered pervasive in natural systems. Maternal effects have been widely studied in vertebrates, especially in the context of social environment, and are often mediated by steroid hormone (SH) deposition to eggs. In insects, although many species dramatically alter phenotype and life‐history traits in response to social density, the mechanisms of these alterations, and the role of hormone deposition by insect mothers into their eggs, remains unknown. In the experiments described here, we assess the effects of social environment on maternal hormone deposition to eggs in house crickets (Acheta domesticus). Specifically, we tested the hypotheses that variable deposition of ecdysteroid hormones (ESH) to eggs is affected by both maternal (a) social density and (b) social composition. We found that while maternal hormone deposition to eggs does not respond to social composition (sex ratio), it does reflect social density; females provision their eggs with higher ESH doses under low‐density conditions. This finding is consistent with the interpretation that variable ESH provisioning is an adaptive maternal response to social environment and congruent with similar patterns of variable maternal provisioning across the tree of life. Moreover, our results confirm that maternal hormone provisioning may mediate delayed density dependence by introducing a time lag in the response of offspring phenotype to population size. Here we show that female crickets respond to social density in provisioning their eggs with hormones that govern hatchling growth and development. This is the first evidence that we are aware of for hormone provisioning as a mechanism for achieving delayed density dependence in a population.

Transgenerational plasticity (TGP) occurs when the environment experienced by a parent influences the development of their offspring. In this article, we develop a framework for understanding the mechanisms and multigenerational consequences of TGP. First, we conceptualize the mechanisms of TGP in the context of communication between parents (senders) and offspring (receivers) by dissecting the steps between an environmental cue received by a parent and its resulting effects on the phenotype of one or more future generations. Breaking down the problem in this way highlights the diversity of mechanisms likely to be involved in the process. Second, we review the literature on multigenerational effects and find that the documented patterns across generations are diverse. We categorize different multigenerational patterns and explore the proximate and ultimate mechanisms that can generate them. Throughout, we highlight opportunities for future work in this dynamic and integrative area of study.

The consequences of early developmental conditions for performance in later life are now subjected to convergent interest from many different biological sub-disciplines. However, striking data, largely from the biomedical literature, show that environmental effects experienced even before conception can be transmissible to subsequent generations. Here, we review the growing evidence from natural systems for these cross-generational effects of early life conditions, showing that they can be generated by diverse environmental stressors, affect offspring in many ways and can be transmitted directly or indirectly by both parental lines for several generations. In doing so, we emphasize why early life might be so sensitive to the transmission of environmentally induced effects across generations. We also summarize recent theoretical advancements within the field of developmental plasticity, and discuss how parents might assemble different ‘internal’ and ‘external’ cues, even from the earliest stages of life, to instruct their investment decisions in offspring. In doing so, we provide a preliminary framework within the context of adaptive plasticity for understanding inter-generational phenomena that arise from early life conditions.

Maternal effects can adaptively modulate offspring developmental trajectories in variable but predictable environments. Hormone synthesis is sensitive to environmental factors, and maternal hormones are thus a powerful mechanism to transfer environmental cues to the next generation. Birds have become a key model for the study of hormone-mediated maternal effects because the embryo develops outside the mother's body, facilitating the measurement and manipulation of prenatal hormone exposure. At the same time, birds are excellent models for the integration of both proximate and ultimate approaches, which is key to a better understanding of the evolution of hormone-mediated maternal effects. Over the past two decades, a surge of studies on hormone-mediated maternal effects has revealed an increasing number of discrepancies. In this review, we discuss the role of the environment, genetic factors and social interactions in causing these discrepancies and provide a framework to resolve them. We also explore the largely neglected role of the embryo in modulating the maternal signal, as well as costs and benefits of hormone transfer and expression for the different family members. We conclude by highlighting fruitful avenues for future research that have opened up thanks to new theoretical insights and technical advances in the field. This article is part of the theme issue ‘Developing differences: early-life effects and evolutionary medicine’.

Summary For most organisms, early life‐history stages are the most sensitive to environmental stress and so transgenerational phenotypic plasticity, whereby the parental environment and offspring environment interact to alter the phenotype of the offspring, is viewed as key to promoting persistence in the face of environmental change. While there has been long‐standing interest in the role of transgenerational plasticity via the maternal line (traditionally the field of maternal effects), increasingly it appears that paternal effects can also play a role. Despite the emerging role of paternal effects in studies of global change, key knowledge gaps remain: first, whether paternal effects act to increase or decrease offspring performance remains largely unexplored; second, the relative roles of maternal and paternal effects are rarely disentangled; and third, the role of environmental variation, a key determinant of the benefits of transgenerational plasticity, has not been explored with regard to paternal effects. Here, we explore all three issues using the marine tubeworm Galeolaria caespitosa, an important habitat‐forming species in southern Australia. We found that both paternal and maternal experiences affected key stages of offspring performance (fertilization and larval development) and, surprisingly, paternal effects were often stronger than maternal effects. Furthermore, we found that paternal effects often reduced offspring performance, especially when environments varied compared with when environments were stable. Our results suggest that, while transgenerational plasticity may play an important role in modifying the impacts of global change, these effects are not uniformly positive. Importantly, paternal effects can be as strong, or stronger, than maternal effects and environmental variability strongly alters the impacts of paternal effects. Lay Summary

Modern evolutionary biology is founded on the Mendelian-genetic model of inheritance, but it is now clear that this model is incomplete. Empirical evidence shows that environment (encompassing all external influences on the genome) can impose transgenerational effects and generate heritable variation for a broad array of traits in animals, plants, and other organisms. Such effects can be mediated by the transmission of epigenetic, cytoplasmic, somatic, nutritional, environmental, and behavioral variation. Building on the work of many authors, we outline a general framework for conceptualizing nongenetic inheritance and its evolutionary implications. This framework shows that, by decoupling phenotypic change from the genotype, nongenetic inheritance can circumvent the limitations of genetic inheritance and thereby influence population dynamics and alter the fitness landscape. The weight of theory and empirical evidence indicates that nongenetic inheritance is a potent factor in evolution that can engender outcomes unanticipated under the Mendelian-genetic model.

Parental brood care greatly affects offspring’s fitness, but the specific effects of care on the collective behaviour of independent offspring are less well understood. It has been suggested that the loss of care induces increased sibling cooperation to compensate parental contributions. However, the empirical evidence is ambiguous. Here, we examined how the loss of early parental care affects the collective behaviour, i.e. shoaling performance of independent juveniles in a genetically heterogeneous lab-population of the biparental cichlid fish Pelvicachromis pulcher. Applying a split-clutch design, we reared in- and outbred offspring with or without parents. In the experiment, we examined shoal density (inter-individual distance) in relation to body size of the shoaling fish. Dense shoaling reduces predation risk and small fish may benefit strongest because they are particularly vulnerable to predation by gape-limited predators. Juveniles reared without parents formed denser shoals and they adjusted shoaling behaviour depending on own body size compared to juveniles reared with parents; especially smaller fish formed dense shoals. Inbreeding did not significantly affect shoaling performance. This indicates that juveniles compensate missing parental care by adjusting their shoaling behaviour depending on own vulnerability. Our study contributes to the understanding of the co-evolution of brood care and sibling cooperation.Significance statementLiving in groups reduces individual predation risk and in fishes, tighter shoals provide better protection than more lose shoals. Here, we examined how the loss of parental care influences the shoaling behaviour of the independent juveniles in the biparental cichlid fish Pelvicachromis pulcher. We show that juveniles that were reared without parents, and especially the most vulnerable, small fish, formed denser shoals compared to juveniles that received care. The results suggest that parental deprivation leads to more pronounced shoaling in the offspring, which may contribute to compensate missing care.

Plant and animal parents may respond to environmental conditions such as resource stress by altering traits of their offspring via heritable non-genetic effects. While such transgenerational plasticity can result in progeny phenotypes that are functionally pre-adapted to the inducing environment, it is unclear whether such parental effects measurably enhance the adult competitive success and lifetime reproductive output of progeny, and whether they may also adversely affect fitness if offspring encounter contrasting conditions. In glasshouse experiments with inbred genotypes of the annual plant Polygonum persicaria , we tested the effects of parental shade versus sun on (a) competitive performance of progeny in shade, and (b) lifetime reproductive fitness of progeny in three contrasting treatments. Shaded parents produced offspring with increased fitness in shade despite competition, as well as greater competitive impact on plant neighbours. Inherited effects of parental light conditions also significantly altered lifetime fitness: parental shade increased reproductive output for progeny in neighbour and understorey shade, but decreased fitness for progeny in sunny, dry conditions. Along with these substantial adaptive and maladaptive transgenerational effects, results show complex interactions between genotypes, parent environment and progeny conditions that underscore the role of environmental variability and change in shaping future adaptive potential. This article is part of the theme issue ‘The role of plasticity in phenotypic adaptation to rapid environmental change’.

There is renewed interest in how transgenerational environmental effects, including epigenetic inheritance, contribute to adaptive evolution. The contribution of across-generation plasticity to adaptation, however, needs to be evaluated within the context of within-generation plasticity, which is often proposed to contribute more efficiently to adaptation because of the potentially greater accuracy of progeny than parental cues to predict progeny selective environments. We highlight recent empirical studies of transgenerational plasticity, and find that they do not consistently support predictions based on the higher predictive ability of progeny environmental cues.Wediscuss these findings within the context of the relative predictive ability of maternal and progeny cues, costs and constraints of plasticity in parental and progeny generations, and the dynamic nature of the adaptive value of within- and across-generation plasticity that varies with the process of adaptation itself. Such contingent and dynamically variable selection could account for the diversity of patterns of within- and across-generation plasticity observed in nature, and can influence the adaptive value of the persistence of environmental effects across generations.