Weak evidence for anticipatory parental effects in plants and animals

The evolution of adaptive phenotypic plasticity relies on the presence of cues that enable organisms to adjust their phenotype to match local conditions. Although mostly studied with respect to nonsocial cues, it is also possible that parents transmit information about the environment to their offspring. Such ‘anticipatory parental effects’ or ‘adaptive transgenerational plasticity’ can have important consequences for the dynamics and adaptive potential of populations in heterogeneous environments. Yet, it remains unknown how widespread this form of plasticity is. Using a meta‐analysis of experimental studies with a fully factorial design, we show that there is only weak evidence for higher offspring performance when parental and offspring environments are matched compared with when they are mismatched. Estimates of heterogeneity among studies suggest that effects, when they occur, are subtle. Study features, environmental context, life stage and trait categories all failed to explain significant amounts of variation in effect sizes. We discuss theoretical and methodological reasons for the limited evidence for anticipatory parental effects and suggest ways to improve our understanding of the prevalence of this form of plasticity in nature.     

Multiple simultaneous treatments change plant response from adaptive parental effects to within‐generation plasticity,in Arabidopsis thaliana

In general, studies on plant phenotypic plasticity concentrate on plant responses to different levels of a single environmental factor. Under natural conditions, however, multiple environmental factors often vary simultaneously. I studied the consequences for lifetime fitness caused by single treatments or treatment combinations by investigating patterns of phenotypic plasticity within and between generations. The parental plants (three genotypes of the annual plant Arabidopsis thaliana) received zero, one or two stress treatments at an early life‐stage. The treatments included wounding, shading, chilling, and their pairwise combinations. In the second generation, offspring of treated plants received either the parental or no treatment. Offspring of non‐treated plants were reared under all treatment conditions. Plants responded strongly to the treatments, especially through delayed reproduction, which positively affected lifetime fitness. Notably, treatment combinations triggered stronger plastic responses on average. Because the delay in reproduction was offset by a delay in senescence, the treatments resulted in a fitness gain instead of a loss. However, under adverse environmental conditions, this delay represents a potential fitness cost, especially when the time for reproduction is limited. The treatments ‘wounding’ and ‘shading’ triggered parental effects that increased fitness only in plants that themselves received the treatment. Untreated offspring of wounded or shaded parents performed like control plants. Also, these parental effects were not accompanied by potential fitness costs, such as delayed reproduction. Chilling triggered genotype‐specific parental effects that increased or reduced fitness. Of the treatment combinations only ‘wounding’ and ‘shading’ resulted in genotype‐specific parental effects that increased or reduced fitness independently of offspring treatment. These results suggest that the response of annual plants to treatment combinations triggers predominantly within‐generation plastic responses that include potential fitness costs, which cannot be inferred from studies that manipulate environmental factors individually. Therefore, single treatment studies likely underestimate the costs of plasticity in natural environments.     

Niche construction through phenological plasticity: life history dynamics and ecological consequences

The ability of an organism to alter the environment that it experiences has been termed 'niche construction'. Plants have several ways whereby they can determine the environment to which they are exposed at different life stages. This paper discusses three of these: plasticity in dispersal, flowering timing and germination timing. It reviews pathways through which niche construction alters evolutionary and ecological trajectories by altering the selective environment to which organisms are exposed, the phenotypic expression of plastic characters, and the expression of genetic variation. It provides examples whereby niche construction creates positive or negative feedbacks between phenotypes and environments, which in turn cause novel evolutionary constraints and novel life-history expression.     

Population density, body size, and phenotypic plasticity of brood size in a burying beetle

Theory predicts that organisms living in heterogeneous environmentswill exhibit phenotypic plasticity. One trait that may be particularlyimportant in this context is the clutch or brood size becauseit is simultaneously a maternal and offspring characteristic.In this paper, I test the hypothesis that the burying beetle,Nicrophorus orbicollis, adjusts brood size, in part, in anticipationof the reproductive environment of its adult offspring. N. orbicollisuse a small vertebrate carcass as a food resource for theiryoung. Both parents provide parental care and actively regulatebrood size through filial cannibalism. The result is a positivecorrelation between brood size and carcass size. Adult bodysize is an important determinant of reproductive success forboth sexes, but only at higher population densities. I testthree predictions generated by the hypothesis that beetles adjustbrood size in response to population density. First, averageadult body size should vary positively with population density.Second, brood size on a given-sized carcass should be larger(producing more but smaller young) in low-density populationsthan in high-density populations. Third, females should respondadaptively to changes in local population density by producinglarger broods when population density is low and small broodswhen population density is high. All three predictions weresupported using a combination of field and laboratory experiments.These results (1) show that brood size is a phenotypically plastictrait and (2) support the idea that brood size decisions arean intergenerational phenomenon that varies with the anticipatedcompetitive environment of the offspring.     

Pathogen‐induced maternal effects result in enhanced immune responsiveness across generations

Parental investment theory postulates that adults can accurately perceive cues from their surroundings, anticipate the needs of future offspring based on those cues, and selectively allocate nongenetic resources to their progeny. Such context‐dependent parental contributions can result in phenotypically variable offspring. Consistent with these predictions, we show that bacterially exposed Manduca sexta mothers oviposited significantly more variable embryos (as measured by mass, volume, hatching time, and hatching success) relative to naïve and control mothers. By using an in vivo “clearance of infection” assay, we also show that challenged larvae born to heat‐killed‐ or live‐Serratia‐injected mothers, supported lower microbial loads and cleared the infection faster than progeny of control mothers. Our data support the notion that mothers can anticipate the future pathogenic risks and immunological needs of their unborn offspring, providing progeny with enhanced immune protection likely through transgenerational immune priming. Although the inclusion of live Serratia into oocytes does not appear to be the mechanism by which mothers confer protection to their young, other mechanisms, including epigenetic modifications in the progeny due to maternal pathogenic stress, may be at play. The adaptive nature of maternal effects in the face of pathogenic stress provides insights into parental investment, resource allocation, and life‐history theories and highlights the significant role that pathogen‐induced maternal effects play as generators and modulators of evolutionary change.     

Plasticity genes and plasticity costs: a new approach using an Arabidopsis recombinant inbred population

Earlier flowering is triggered by vernalization in some but not all Arabidopsis ecotypes, often reflecting allelic variation at the FRIGIDA (FRI) locus. Using a recombinant inbred (RI) population polymorphic at FRI, we examined fitness consequences of variation for plasticity. Flowering and fitness were scored for 68 RI genotypes following full and partial vernalization treatments. Within-environment and mixed-model anovas estimated variance components for a genotype effect and a G x E term, respectively. Selection analyses examined whether delayed bolting increases fitness; a plasticity costs analysis asked whether increased plasticity lowers fitness. We also explored whether trait QTL had environment-specific effects, colocated in the immediate vicinity of FRI, or overlapped with fitness QTL. Selection may favor fri alleles and constitutive early flowering, especially in conditions that only partially vernalize plants. Plasticity costs, detected only after partial vernalization and only marginally significant, were nonetheless consistent with FRI-FLC function. We discuss how information about QTL with environment-specific effects, fitness QTL, and knowledge about plasticity genes can improve interpretation of selection or plasticity cost analyses.     

克隆和有性亲体效应及其调控机制

植物表型受自身基因型、所处环境及其亲体所经历环境的共同影响;其中,亲体环境对子代表型的影响被称为亲体效应。亲体效应不仅可通过有性繁殖产生的种子传递给后代(即有性亲体效应),也可以通过克隆生长等无性繁殖产生的分株传递给后代(即克隆亲体效应)。亲体效应对植物种群,特别是对有性繁殖受限、缺乏遗传变异的克隆植物种群的长期进化可能发挥着极其重要的作用,因此,对亲体效应研究进展的梳理非常必要。对克隆亲体效应和有性亲体效应的内涵进行了阐释,并论述了克隆和有性亲体效应对子代表型、适合度、种内/种间竞争能力以及种群/群落结构和功能的潜在影响;阐述了亲体效应的潜在调控机制,包括供给机制、代谢物质调控机制、表观遗传机制等;论述了克隆亲体效应在克隆植物适应进化中的作用。未来可以就克隆亲体效应的遗传稳定性及其对克隆生活史性状变异的贡献程度,以及克隆和有性亲体效应引起的表型多样性对种内/种间关系、种群/群落多样性及生态系统结构、功能和稳定性的影响开展深入研究。     

Within- and between-generation effects of temperature on life-history traits in a butterfly

Non-genetic parental effects may largely affect offspring phenotype, and such plasticity is potentially adaptive. Despite its potential importance, little is known about cross-generational effects of temperature, at least partly because parental effects were frequently considered a troublesome nuisance, rather than a target of experimental studies. We here investigate effects of parental, developmental and acclimation temperature on life-history traits in the butterfly Bicyclus anynana. Higher developmental temperatures reduced development times and egg size, increased egg number, but did not affect pupal mass. Between-generation temperature effects on larval time, pupal time, larval growth rate and egg size were qualitatively very similar to effects of developmental temperature, and additionally affected pupal mass but not egg number. Parental effects are important mediators of phenotypic plasticity in B. anynana, and partly yielded antagonistic effects on different components of fitness, which may constrain the evolution of cross-generational adaptive plasticity.     

Plastic responses to parents and predators lead to divergent shoaling behaviour in sticklebacks

Population divergence in antipredator defence and behaviour occurs rapidly and repeatedly. Genetic differences, phenotypic plasticity or parental effects may all contribute to divergence, but the relative importance of each of these mechanisms remains unknown. We exposed juveniles to parents and predators to measure how induced changes contribute to shoaling behaviour differences between two threespine stickleback species (benthics and limnetics: Gasterosteus spp). We found that limnetics increased shoaling in response to predator attacks, whereas benthics did not alter their behaviour. Care by limnetic fathers led to increased shoaling in both limnetic and benthic offspring. Shoaling helps limnetics avoid trout and avian predation; our results suggest that this adaptive behaviour is the result of a combination of paternal effects, predator-induced plasticity and genetic differences between species. These results suggest that plasticity substantially contributes to the rapid divergence in shoaling behaviour across the post-Pleistocene radiation of sticklebacks.     

Parental effects and the evolution of phenotypic memory

Despite growing evidence for nongenetic inheritance, the ecological conditions that favour the evolution of heritable parental or grandparental effects remain poorly understood. Here, we systematically explore the evolution of parental effects in a patch‐structured population with locally changing environments. When selection favours the production of a mix of offspring types, this mix differs according to the parental phenotype, implying that parental effects are favoured over selection for bet‐hedging in which the mixture of offspring phenotypes produced does not depend on the parental phenotype. Positive parental effects (generating a positive correlation between parental and offspring phenotype) are favoured in relatively stable habitats and when different types of local environment are roughly equally abundant, and can give rise to long‐term parental inheritance of phenotypes. By contrast, unstable habitats can favour negative parental effects (generating a negative correlation between parental and offspring phenotype), and under these circumstances, even slight asymmetries in the abundance of local environmental states select for marked asymmetries in transmission fidelity.     

Pleiotropic effects of flowering time genes in the annual crucifer Arabidopsis thaliana (Brassicaceae)

Variation in flowering time of Arabidopsis thaliana was studied in an experiment with mutant lines. The pleiotropic effects of flowering time genes on morphology and reproductive yield were assessed under three levels of nutrient supply. At all nutrient levels flowering time and number of rosette leaves at flowering varied among mutant lines. The relationship between these two traits depended strongly on nutrient supply. A lower nutrient supply first led to an extension of the vegetative phase, while the mean number of leaves at flowering was hardly affected. A further reduction resulted in no further extension of the vegetative phase and, on average, plants started flowering with a lower leaf number. At low nutrients, early flowering affected the timing of production of siliques rather than the total output, whereas late flowering was favorable at high nutrients. This may explain the fact that many plant species flower at a relatively small size under poor conditions. Flowering time genes had pleiotropic effects on the leaf length, number of rosette and cauline leaves, and number of axillary flowering shoots of the main inflorescence. Silique production was positively correlated with the number of axillary shoots of the main inflorescence; the number of axillary primordia appeared to have a large impact on reproductive yield.     

Unique maternal and environmental effects on the body morphology of the Least Killifish,Heterandria formosa

An important step in diagnosing local adaptation is the demonstration that phenotypic variation among populations is at least in part genetically based. To do this, many methods experimentally minimize the environmental effect on the phenotype to elucidate the genetic effect. Minimizing the environmental effect often includes reducing possible environmental maternal effects. However, maternal effects can be an important factor in patterns of local adaptation as well as adaptive plasticity. Here, we report the results of an experiment with males from two populations of the poeciliid fish, Heterandria formosa, designed to examine the relative influence of environmental maternal effects and environmental effects experienced during growth and development on body morphology, and, in addition, whether the balance among those effects is unique to each population. We used a factorial design that varied thermal environment and water chemistry experienced by mothers and thermal environment and water chemistry experienced by offspring. We found substantial differences between the two populations in their maternal and offspring norms of reaction of male body morphology to differences in thermal environment and water chemistry. We also found that the balance between maternal effects and postparturition environmental effects differed from one thermal regime to another and among traits. These results indicate that environmental maternal effects can be decidedly population‐specific and, as a result, might either contribute to the appearance of or blur evidence for local adaptation. These results also suggest that local adaptation might also occur through the evolution of maternal norms of reaction to important, and varying, environmental factors.     

Natural selection acts in opposite ways on correlated hormonal mediators of prenatal maternal effects in a wild bird population

Maternal hormones are important mediators of prenatal maternal effects. Although many experimental studies have demonstrated their potency in shaping offspring phenotypes, we know remarkably little about their adaptive value. Using long‐term data on a wild collared flycatcher (Ficedula albicollis) population, we show that natural selection acts in opposite ways on two maternally derived androgens, yolk androstenedione (A4) and yolk testosterone (T). High yolk A4 concentrations are associated with higher fitness, whereas high yolk T concentrations are associated with lower fitness. Natural selection thus favours females that produce eggs with high A4 and low T concentrations. Importantly, however, there exists a positive (non‐genetic) correlation between A4 and T, which suggests that females are limited in their ability to reach this adaptive optimum. Thereby, these results provide strong evidence for an adaptive value of differential maternal androgen deposition, and a mechanistic explanation for the maintenance of variation in maternal investment in the wild.     

Plasticity to simulated shade is associated with altitude in structured populations of Arabidopsis thaliana

Plants compete for photosynthesis light and induce a shade avoidance syndrome (SAS) that confers an important advantage in asymmetric competition for light at high canopy densities. Shade plasticity was studied in a greenhouse experiment cultivating Arabidopsis thaliana plants from 15 populations spread across an altitudinal gradient in the northeast area of Spain that contain a high genetic variation into a reduced geographical range. Plants were exposed to sunlight or simulated shade to identify the range of shade plasticity. Fourteen vegetative, flowering and reproductive traits were measured throughout the life cycle. Shade plasticity in flowering time and dry mass was significantly associated with the altitude of population origin. Plants from coastal populations showed higher shade plasticity indexes than those from mountains. The altitudinal variation in flowering leaf plasticity adjusted negatively with average and minimum temperatures, whereas dry mass plasticity was better explained by negative regressions with the average, maximum and minimum temperatures, and by a positive regression with average precipitation of the population origin. The lack of an altitudinal gradient for the widest number of traits suggests that shade light could be a driver explaining the distribution pattern of individuals in smaller geographical scales than those explored here.     

Environmental and not maternal effects determine variation in offspring phenotypes in a passerine bird

Maternal and environmental effects can profoundly influence offspring phenotypes, independent of genetic effects. Within avian broods, both the asymmetric post‐hatching environment created by hatching asynchrony and the differential maternal investment through the laying sequence have important consequences for individual nestlings in terms of the allocation of resources to body structures with different contributions to fitness. The purpose of this study was to evaluate the relative importance of post‐hatching environmental and maternal effects in generating variation in offspring phenotypes. First, an observational study showed that within blue tit, Cyanistes caeruleus, broods, late‐hatched nestlings allocated resources to tarsus development, maintained mass gain and head‐bill growth and directed resources away from the development of fourth primary feathers. Second, a hatching order manipulation experiment resulted in nestlings from first‐laid eggs hatching last, thereby allowing comparison with both late and early‐hatched nestlings. Experimental nestlings had growth patterns which were closer to late‐hatched nestlings, suggesting that within‐brood growth patterns are determined by post‐hatching environmental effects. Therefore, we conclude that post‐hatching environmental effects play an important role in generating variation in offspring phenotypes.     

How stabilizing selection and nongenetic inheritance combine to shape the evolution of phenotypic plasticity

Relatively little is known about whether and how nongenetic inheritance interacts with selection to impact the evolution of phenotypic plasticity. Here, we empirically evaluated how stabilizing selection and a common form of nongenetic inheritance—maternal environmental effects—jointly influence the evolution of phenotypic plasticity in natural populations of spadefoot toads. We compared populations that previous fieldwork has shown to have evolved conspicuous plasticity in resource‐use phenotypes (“resource polyphenism”) with those that, owing to stabilizing selection favouring a narrower range of such phenotypes, appear to have lost this plasticity. We show that: (a) this apparent loss of plasticity in nature reflects a condition‐dependent maternal effect and not a genetic loss of plasticity, that is “genetic assimilation,” and (b) this plasticity is not costly. By shielding noncostly plasticity from selection, nongenetic inheritance generally, and maternal effects specifically, can preclude genetic assimilation from occurring and consequently impede adaptive (genetic) evolution.     

Maternal predator-exposure has lifelong consequences for offspring learning in threespined sticklebacks

Learning is an important form of phenotypic plasticity that allows organisms to adjust their behaviour to the environment. An individual''s learning performance can be affected by its mother''s environment. For example, mothers exposed to stressors, such as restraint and forced swimming, often produce offspring with impaired learning performance. However, it is unclear whether there are maternal effects on offspring learning when mothers are exposed to ecologically relevant stressors, such as predation risk. Here, we examined whether maternal predator-exposure affects adult offsprings’ learning of a discrimination task in threespined sticklebacks (Gasterosteus aculeatus). Mothers were either repeatedly chased by a model predator (predator-exposed) or not (unexposed) while producing eggs. Performance of adult offspring from predator-exposed and unexposed mothers was assessed in a discrimination task that paired a particular coloured chamber with a food reward. Following training, all offspring learned the colour-association, but offspring of predator-exposed mothers located the food reward more slowly than offspring of unexposed mothers. This pattern was not driven by initial differences in exploratory behaviour. These results demonstrate that an ecologically relevant stressor (predation risk) can induce maternal effects on offspring learning, and perhaps behavioural plasticity more generally, that last into adulthood.     

Separating parental environment from seed size effects on next generation growth and development in Arabidopsis

Plant growth and development is profoundly influenced by environmental conditions that laboratory experimentation typically attempts to control. However, growth conditions are not uniform between or even within laboratories and the extent to which these differences influence plant growth and development is unknown. Experiments with wild-type Arabidopsis thaliana were designed to quantify the influences of parental environment and seed size on growth and development in the next generation. A single lot of seed was planted in six environmental chambers and grown to maturity. The seed produced was mechanically sieved into small and large size classes then grown in a common environment and subjected to a set of assays spanning the life cycle. Analysis of variance demonstrated that seed size effects were particularly significant early in development, affecting primary root growth and gravitropism, but also flowering time. Parental environment affected progeny germination time, flowering and weight of seed the progeny produced. In some cases, the parental environment affected the magnitude of (interacted with) the observed seed size effects. These data indicate that life history circumstances of the parental generation can affect growth and development throughout the life cycle of the next generation to an extent that should be considered when performing genetic studies.