Anticipatory Maternal Effects Research Articles

Predictability of parental ultraviolet-B environment shapes the growth strategies of clonal Glechoma longituba

Although there is an increasing debate about ecological consequences of environmental predictability for plant phenotype and fitness, the effect of predictability of parental environments on the offspring is still indefinite. To clarify the role of environmental predictability in maternal effects and the growth strategy of clonal offspring, a greenhouse experiment was conducted with Glechoma longituba. The parental ramets were arranged in three ultraviolet-B (UV-B) conditions, representing two predictable environments (regular and enhanced UV-B) and an unpredictable environment (random UV-B), respectively. The offspring environments were the same as their parent or not (without UV-B). At the end of experiment, the growth parameters of offspring were analyzed. The results showed that maternal effects and offspring growth were regulated by environmental predictability. Offspring of unpredictable environmental parents invested more resources in improving defense components rather than in rapid growth. Although offspring of predictable parents combined two processes of defense and growth, there were still some differences in the strategies between the two offspring, and the offspring of regular parent increased the biomass allocation to roots (0.069 g of control vs. 0.092 g of regular), but that of enhanced parent changed the resource allocation of nitrogen in roots and phosphorus in blade. Moreover, when UV-B environments of parent and offspring were matched, it seemed that maternal effects were not adaptive, while the growth inhibition in the predictable environment was weaker than that in unpredictable environment. In the predictable environment, the recovered R/S and the increased defense substances (flavonoid and anthocyanin) contributed to improving offspring fitness. In addition, when UV-B environments of parent and offspring were mismatched, offspring growth was restored or improved to some extent. The offspring performance in mismatched environments was controlled by both transgenerational effect and within-generational plasticity. In summary, the maternal effects affected growth strategies of offspring, and the differences of strategies depended on the predictability of parental UV-B environments, the clone improved chemical defense to cope with unpredictable environments, while the growth and defense could be balanced in predictable environments. The anticipatory maternal effects were likely to improve the UV-B resistance.

Adaptive Maternal Effects Shape Offspring Phenotype and Survival in Natal Environments.

AbstractMaternal effects can give newborns a head start in life by adjusting natal phenotypes to natal environments, yet their strength and adaptiveness are often difficult to investigate in natural populations. Here, we studied anticipatory maternal effects and their adaptiveness in common lizards in a seminatural experimental system. Specifically, we investigated how maternal environments (i.e., vegetation cover) and maternal phenotype (i.e., activity levels and body length) can shape offspring phenotype. We further studied whether such maternal effects influenced offspring survival in natal environments varying with respect to vegetation cover, conspecific density, and, consequently, maternal fitness. More active females from dense vegetation habitats produced bigger offspring than their less active counterparts, the contrary being true for sparse vegetation habitats. Moreover, females from dense vegetation habitats produced more active offspring and more active offspring survived better in dense vegetation habitats, resulting in greater maternal fitness through maternal effects. These results suggest adaptive anticipatory maternal effects, induced by vegetation structure and mediated by activity levels that may shape early-life prospects in natal environments.

Effects of elevated temperature on reproduction and larval settlement in Leptastrea purpurea.

As global ocean temperatures continue to rise, severe declines in coral reef health and diversity are reported on a global scale. Recovery of coral reefs relies on reproduction and increased rates of successful recruitment, which can vary tremendously across coral species. We investigated the effects of increased temperatures in the environment of parental colonies on larval production, size, settlement and survival, in the heat-resistant coral Leptastrea purpurea in Guam. Thanks to two tank experiments (eleven and four weeks, respectively) conducted over two consecutive years we found that larvae released by heat-treated parents (30 °C) were significantly smaller in size but greater in number, had normal settlement behavior and increased post-settlement survival rates compared to those released by control parent colonies (28 °C). We conclude that changes in the environment of parental L. purpurea colonies trigger an anticipatory maternal effect which leads to the release of preconditioned larvae with an increased chance of survival.Supplementary InformationThe online version contains supplementary material available at 10.1007/s00338-022-02241-y.

Environmental variation mediates the evolution of anticipatory parental effects.

Theory maintains that when future environment is predictable, parents should adjust the phenotype of their offspring to match the anticipated environment. The plausibility of positive anticipatory parental effects is hotly debated and the experimental evidence for the evolution of such effects is currently lacking. We experimentally investigated the evolution of anticipatory maternal effects in a range of environments that differ drastically in how predictable they are. Populations of the nematode Caenorhabditis remanei, adapted to 20°C, were exposed to a novel temperature (25°C) for 30 generations with either positive or zero correlation between parent and offspring environment. We found that populations evolving in novel environments that were predictable across generations evolved a positive anticipatory maternal effect, because they required maternal exposure to 25°C to achieve maximum reproduction in that temperature. In contrast, populations evolving under zero environmental correlation had lost this anticipatory maternal effect. Similar but weaker patterns were found if instead rate‐sensitive population growth was used as a fitness measure. These findings demonstrate that anticipatory parental effects evolve in response to environmental change so that ill‐fitting parental effects can be rapidly lost. Evolution of positive anticipatory parental effects can aid population viability in rapidly changing but predictable environments.

Filial egg cannibalism in the European earwig: its determinants and implications in the evolution of maternal egg care

In many animal species, mothers eat some of their own eggs. While this filial egg cannibalism can have profound impacts on both parental and offspring fitness, it remains unclear whether this behaviour is a simple by-product of a generally low maternal investment in egg care and whether it is determined before or after egg production. Here, we addressed these questions in the European earwig, Forficula auricularia, an insect in which females vary in their level of investment in egg care and in their expression of egg cannibalism. Using a cross-fostering experiment, we investigated the benefits of egg cannibalism for mothers, the potential association between egg cannibalism and egg care, and whether egg cannibalism is a maternal strategy that is determined before or after egg laying. Our results first revealed that egg cannibalism provided direct benefits to mothers, as the females that consumed some of their eggs increased their investment in future reproduction. We then showed that egg cannibalism was independent of the level of maternal investment in two important forms of egg care (egg defence and the time taken to return after a simulated predator attack). Overall, this suggests that access to egg cannibalism may select for mothers to remain with their eggs, independent of the potential benefits of care for the eggs. Finally, we demonstrated that the number of eggs received, but not the number of eggs produced by foster mothers, determined the level of egg cannibalism. This highlights that egg cannibalism is determined after egg laying and is not the outcome of anticipatory maternal effects. Overall, these findings provide novel insights into our understanding of the early evolution of parental care, as they suggest that the direct benefits of filial egg cannibalism for mothers could have promoted egg attendance from an ancestral egg abandonment state. • Filial egg cannibalism has profound impacts on both parental and offspring fitness. • European earwig mothers benefited directly from eating some of their eggs. • Egg cannibalism was independent of the level of maternal investment. • It is determined after egg laying and is not an anticipatory maternal effect. • It is not a simple by-product of a low maternal investment in care.

Between- and Within-Individual Variation of Maternal Thyroid Hormone Deposition in Wild Great Tits (Parus major).

Maternal hormones are often considered a mediator of anticipatory maternal effects; namely, mothers adjust maternal hormone transfer to prepare the offspring for the anticipated environment. The flexibility for mothers to adjust hormone transfer is therefore a prerequisite for such anticipatory maternal effects. Nevertheless, previous studies have focused only on the average differences of maternal hormone transfer between groups and neglected the substantial individual variation, despite the fact that individual plasticity in maternal hormone transfer is actually the central assumption. In this study, we studied the between- and within-individual variation of maternal thyroid hormones (THs) in egg yolk of wild great tits (Parus major) and estimated the individual plasticity of maternal yolk THs across environmental temperature, clutch initiation dates, and egg laying order using linear mixed effects models. Interestingly, our models provide statistical evidence that the two main THs-the main biologically active hormone T3 and T4, which is mostly considered a prohormone-exhibited different variation patterns. Yolk T3 showed significant between-individual variation on the average levels, in line with its previously reported moderate heritability. Yolk T4, however, showed significant between-clutch variation in the pattern over the laying sequence, suggesting a great within-individual plasticity. Our findings suggest that the role and function of the hormone within the endocrine axis likely influences its flexibility to respond to environmental change. Whether the flexibility of T4 deposition brings a fitness advantage should be examined along with its potential effects on offspring, which remain to be further investigated.

Maternal effects obscure condition-dependent sex allocation in changing environments.

Climate change increases environmental fluctuations which thereby impact population demography. Species with temperature-dependent sex determination may experience more extreme sex ratio skews, but this has not been considered in species with chromosomally determined sex. However, anticipatory maternal effects cause lifelong physiological changes impacting sex ratios. Here we show, in mice, that more sons were born to mothers in good condition when their breeding environment matched their gestational environment, consistent with theoretical predictions, but mothers in mismatched environments have no condition–sex ratio relationship. Thus, the predicted effect of condition on sex ratio was obscured by maternal effects when the environment changed. This may explain extreme sex ratio skews in reintroduced or translocated populations, and sex ratio skews may become more common and less predictable with accelerating environmental change.

Low food availability during gestation enhances offspring post-natal growth, but reduces survival, in a viviparous lizard.

The environment experienced by a mother can have profound effects on the fitness of her offspring (i.e., maternal effects). Maternal effects can be adaptive when the developmental environments experienced by offspring promote phenotypes that provide fitness benefits either via matching offspring phenotype to the post-developmental environment (also known as anticipatory maternal effects) or through direct effects on offspring growth and survival. We tested these hypotheses in a viviparous lizard using a factorial experimental design in which mothers received either high or low amounts of food during gestation, and resultant offspring were raised on either high or low amounts of food post-birth. We found no effect of food availability during gestation on reproductive traits of mothers or offspring traits at birth. However, offspring from mothers who received low food during gestation exhibited a greater increase in condition in the post-birth period, suggesting some form of priming of offspring by mothers to cope with an anticipated poor environment after birth. Offspring that received low food during gestation were also more likely to die, suggesting a trade-off for this accelerated growth. There were also significant effects of post-birth food availability on offspring snout-vent length and body condition growth, with offspring with high food availability post birth doing better. However, the effects of thepre- and post-natal resource evnironment on offspring growth were independent on one another, therefore, providing no support for the presence of anticipatory maternal effects in the traditional sense.

Timing of maternal exposure to toxic cyanobacteria and offspring fitness in Daphnia magna: Implications for the evolution of anticipatory maternal effects.

Organisms that regularly encounter stressful environments are expected to use cues to develop an appropriate phenotype. Water fleas (Daphnia spp.) are exposed to toxic cyanobacteria during seasonal algal blooms, which reduce growth and reproductive investment. Because generation time is typically shorter than the exposure to cyanobacteria, maternal effects provide information about the local conditions subsequent generations will experience. Here, we evaluate if maternal effects in response to microcystin, a toxin produced by cyanobacteria, represent an inheritance system evolved to transmit information in Daphnia magna. We exposed mothers as juveniles and/or as adults, and tested the offspring's fitness in toxic and non‐toxic environments. Maternal exposure until reproduction reduced offspring fitness, both in the presence and in the absence of toxic cyanobacteria. However, this effect was accompanied by a small positive fitness effect, relative to offspring from unexposed mothers, in the presence of toxic cyanobacteria. This effect was mainly elicited in response to maternal exposure to toxic cyanobacteria early in life and less so during reproduction. None of these effects were explained by changes in egg size. A meta‐analysis using our and others’ experiments suggests that the adaptive value of maternal effects to cyanobacteria exposure is weak at best. We suggest that the beneficial maternal effect in our study is an example of phenotypic accommodation spanning generations, rather than a mechanism evolved to transmit information about cyanobacteria presence between generations.

Maternal Effects Via Resting eggs in Predator Defense of the Rotifer Brachionus calyciflorus.

Maternal effects play important evolutionary and ecological roles. Amictic female mothers of monogonont rotifer Brachionus calyciflorus can transmit predatory information of Asplanchna brightwellii in their environment to their offspring by changing the offspring's defensive morphology to increase their fitness. However, it remains unclear whether such maternal effects also exist during sexual reproduction of a mictic mother. This study explored the maternal effect in mictic mothers using the B. calyciflorus and A. brightwellii as a prey-predator model. We collected resting eggs from two groups of mictic mothers that previously experienced environments with (P environment) or without (NP environment) Asplanchna kairomones. Stem females from the resting eggs of each maternal group were also hatched and reared in P and NP environments. The population growth rate of offspring who experienced the same environment as their mictic mothers was significantly higher than those that experienced a different environment. When exposed to a gradient of predator kairomone levels, the posterolateral spine of the offspring elongated with increasing kairomone concentration. Offspring from the P mictic mother showed significantly shorter posterolateral spines than those from the NP mictic mother at each predator kairomone level. Offspring originating from NP mictic mothers clearly elongated their posterolateral spines at low concentrations of predator kairomones, while those from P mothers elongated their posterolateral spines only at the highest levels of predator kairomone. Our findings highlight the existence of anticipatory maternal effects during the sexual process via resting eggs of B. calyciflorus in response to predator kairomone.

Prenatal maternal effects appear to be insensitive to experimental or natural environmental variation

SummaryIn many birds, hatching asynchrony is a common phenomenon, primarily driven by patterns of incubation behaviour. However, experimental results in blue tits (Cyanistes caeruleus) have shown that asynchrony is reduced by intrinsic properties of later eggs that accelerate prenatal development.These intrinsic differences between early and late eggs could be driven by changes in resource availability to females, which are then passively passed onto the egg. Alternatively, it may be due to an anticipatory maternal effect, wherein some signal or resource is actively placed within the egg, which is beneficial to those eggs laid late within the clutch.In order to distinguish between these hypotheses we designed a supplementary feeding experiment, wherein females were provided with food at certain times during the laying phase. This had no discernible effect on development rate, or other egg characteristics, consistent with anticipatory maternal effects.Using a larger dataset we also tested whether natural environmental variation (weather) during egg formation affected maternal investment in eggs. Similarly, egg characteristics were found to be relatively insensitive to the environmental variation, supporting the experimental results.Alay summaryis available for this article.

Maternal programming of offspring in relation to food availability in an insect (Forficula auricularia).

Maternal effects can induce adjustments in offspring phenotype to the environment experienced by the mother. Of particular interest is if mothers can programme their offspring to cope best under matching environmental conditions, but the evidence for such anticipatory maternal effects (AME) is limited. In this study, we manipulated experimentally the food availability experienced by mothers and their offspring in the European earwig (Forficula auricularia). Offspring produced by females that had access to high or low food quantities were cross-fostered to foster mothers experiencing matched or mismatched environments. Offspring experiencing food availability matching the one of their mothers had an increased survival to adulthood compared with offspring experiencing mismatched conditions. Females experiencing high food laid larger clutches. This clutch-size adjustment statistically explained the matching effect when offspring experienced high food, but not when experiencing low food conditions. There were no effects of matching on offspring growth and developmental rate. Overall, our study demonstrates that AME occurs in relation to food availability enhancing offspring survival to adulthood under matching food conditions.

Adaptation to Temporally Fluctuating Environments by the Evolution of Maternal Effects.

All organisms live in temporally fluctuating environments. Theory predicts that the evolution of deterministic maternal effects (i.e., anticipatory maternal effects or transgenerational phenotypic plasticity) underlies adaptation to environments that fluctuate in a predictably alternating fashion over maternal-offspring generations. In contrast, randomizing maternal effects (i.e., diversifying and conservative bet-hedging), are expected to evolve in response to unpredictably fluctuating environments. Although maternal effects are common, evidence for their adaptive significance is equivocal since they can easily evolve as a correlated response to maternal selection and may or may not increase the future fitness of offspring. Using the hermaphroditic nematode Caenorhabditis elegans, we here show that the experimental evolution of maternal glycogen provisioning underlies adaptation to a fluctuating normoxia–anoxia hatching environment by increasing embryo survival under anoxia. In strictly alternating environments, we found that hermaphrodites evolved the ability to increase embryo glycogen provisioning when they experienced normoxia and to decrease embryo glycogen provisioning when they experienced anoxia. At odds with existing theory, however, populations facing irregularly fluctuating normoxia–anoxia hatching environments failed to evolve randomizing maternal effects. Instead, adaptation in these populations may have occurred through the evolution of fitness effects that percolate over multiple generations, as they maintained considerably high expected growth rates during experimental evolution despite evolving reduced fecundity and reduced embryo survival under one or two generations of anoxia. We develop theoretical models that explain why adaptation to a wide range of patterns of environmental fluctuations hinges on the existence of deterministic maternal effects, and that such deterministic maternal effects are more likely to contribute to adaptation than randomizing maternal effects.

Reproduction in Risky Environments: The Role of Invasive Egg Predators in Ladybird Laying Strategies.

Reproductive environments are variable and the resources available for reproduction are finite. If reliable cues about the environment exist, mothers can alter offspring phenotype in a way that increases both offspring and maternal fitness (‘anticipatory maternal effects’—AMEs). Strategic use of AMEs is likely to be important in chemically defended species, where the risk of offspring predation may be modulated by maternal investment in offspring toxin level, albeit at some cost to mothers. Whether mothers adjust offspring toxin levels in response to variation in predation risk is, however, unknown, but is likely to be important when assessing the response of chemically defended species to the recent and pervasive changes in the global predator landscape, driven by the spread of invasive species. Using the chemically defended two-spot ladybird, Adalia bipunctata, we investigated reproductive investment, including egg toxin level, under conditions that varied in the degree of simulated offspring predation risk from larval harlequin ladybirds, Harmonia axyridis. H. axyridis is a highly voracious alien invasive species in the UK and a significant intraguild predator of A. bipunctata. Females laid fewer, larger egg clusters, under conditions of simulated predation risk (P+) than when predator cues were absent (P-), but there was no difference in toxin level between the two treatments. Among P- females, when mean cluster size increased there were concomitant increases in both the mass and toxin concentration of eggs, however when P+ females increased cluster size there was no corresponding increase in egg toxin level. We conclude that, in the face of offspring predation risk, females either withheld toxins or were physiologically constrained, leading to a trade-off between cluster size and egg toxin level. Our results provide the first demonstration that the risk of offspring predation by a novel invasive predator can influence maternal investment in toxins within their offspring.

Trans-generational plasticity in physiological thermal tolerance is modulated by maternal pre-reproductive environment in the polychaeteOphryotrocha labronica

Maternal temperature is known to affect many aspects of offspring phenotype, but its effect on offspring physiological thermal tolerance has received less attention, despite the importance of physiological traits in defining organismal ability to cope with temperature changes. To fill this gap, we used the marine polychaete Ophryotrocha labronica to investigate the influence of maternal temperature on offspring upper and lower thermal tolerance limits, and assess whether maternal influence changed according to the stage of offspring pre-zygotic development at which a thermal cue was provided. Measurements were taken on adult offspring acclimated to 18 or 30°C, produced by mothers previously reared at 24°C and then exposed to 18 or 30°C at an early and late stage of oogenesis. When the shift from 24°C was provided early during oogenesis, mothers produced offspring with greater cold and heat tolerance whenever mother-offspring temperatures did not match, with respect to when they matched, suggesting the presence of an anticipatory maternal effect triggered by the thermal variation. Conversely, when the cue was provided later during oogenesis, more tolerant offspring were observed when temperatures persisted across generations. In this case, maternal exposure to 18 or 30°C may have benefited offspring performance, while limitations in the transmission of the thermal cue may account for the lack of correlation between maternal experiences and offspring performance when mother-offspring environments did not match. Our results provided evidence for a trans-generational effect of temperature on physiological performance characterised by a high context dependency, and are discussed in the light of maternal pre-reproductive experiences.

Seed dimorphism, nutrients and salinity differentially affect seed traits of the desert halophyte Suaeda aralocaspicavia multiple maternal effects

BackgroundMaternal effects may influence a range of seed traits simultaneously and are likely to be context-dependent. Disentangling the interactions of plant phenotype and growth environment on various seed traits is important for understanding regeneration and establishment of species in natural environments. Here, we used the seed-dimorphic plant Suaeda aralocaspica to test the hypothesis that seed traits are regulated by multiple maternal effects.ResultsPlants grown from brown seeds had a higher brown:black seed ratio than plants from black seeds, and germination percentage of brown seeds was higher than that of black seeds under all conditions tested. However, the coefficient of variation (CV) for size of black seeds was higher than that of brown seeds. Seeds had the smallest CV at low nutrient and high salinity for plants from brown seeds and at low nutrient and low salinity for plants from black seeds. Low levels of nutrients increased size and germinability of black seeds but did not change the seed morph ratio or size and germinability of brown seeds. High levels of salinity decreased seed size but did not change the seed morph ratio. Seeds from high-salinity maternal plants had a higher germination percentage regardless of level of germination salinity.ConclusionsOur study supports the multiple maternal effects hypothesis. Seed dimorphism, nutrient and salinity interacted in determining a range of seed traits of S. aralocaspica via bet-hedging and anticipatory maternal effects. This study highlights the importance of examining different maternal factors and various offspring traits in studies that estimate maternal effects on regeneration.

Adaptive significance of temperature-induced egg size plasticity in a planktonic rotifer, Brachionus calyciflorus

Larger egg size and body size at lower temperature are widely observed in zooplankton and other groups. Theoretically, considering the increased cost of producing larger eggs, females would produce larger and fewer eggs only if the newborn from such eggs perform better under certain environmental constraints, such as low temperature. In temperate lakes, low water temperature is a fairly reliable cue of future declining dietary conditions for herbivorous zooplankters. Under these conditions, females that produce more resistant offspring are likely to be selected. Nevertheless, it is not efficient for them to do this at high temperature, when the dietary conditions are usually more abundant. In this study, the adaptive significance of temperature-induced plasticity in a planktonic rotifer, Brachionus calyciflorus, was investigated. We found that: first, the egg size and body size were negatively related to temperature; second, neonates from larger eggs induced by low a temperature of 138C were more resistant to starvation at three different experimental temperatures; third, life table experiments showed that offspring from larger eggs had a higher population growth rate and shorter juvenile period than those from smaller ones at low temperature, and vice versa, which suggests that this may be attributed to some form of anticipatory maternal effect. These differences in population growth rates were mainly due to higher fertility during the first 1 or 2 days after maturation. All of these findings support the view that temperature-induced egg size plasticity has adaptive significance in rotifers.

Mothers Matter Too: Benefits of Temperature Oviposition Preferences in Newts

The maternal manipulation hypothesis states that ectothermic females modify thermal conditions during embryonic development to benefit their offspring (anticipatory maternal effect). However, the recent theory suggests that the ultimate currency of an adaptive maternal effect is female fitness that can be maximized also by decreasing mean fitness of individual offspring. We evaluated benefits of temperature oviposition preferences in Alpine newts (Ichthyosaura [formerly Triturus] alpestris) by comparing the thermal sensitivity of maternal and offspring traits across a range of preferred oviposition temperatures (12, 17, and 22°C) and by manipulating the egg-predation risk during oviposition in a laboratory thermal gradient (12–22°C). All traits showed varying responses to oviposition temperatures. Embryonic developmental rates increased with oviposition temperature, whereas hatchling size and swimming capacity showed the opposite pattern. Maternal oviposition and egg-predation rates were highest at the intermediate temperature. In the thermal gradient, females oviposited at the same temperature despite the presence of caged egg-predators, water beetles (Agabus bipustulatus). We conclude that female newts prefer a particular temperature for egg-deposition to maximize their oviposition performance rather than offspring fitness. The evolution of advanced reproductive modes, such as prolonged egg-retention and viviparity, may require, among others, the transition from selfish temperature preferences for ovipositon to the anticipatory maternal effect.

Anticipatory maternal effects in two different clones of Daphnia magna in response to food shortage

The effects of food shortage on growth, fecundity, male production and offspring size and starvation tolerance in two different clones of Daphnia magna (Clone L and Clone P) were evaluated by disentangling the effects of resource depletion and crowding per se. Three experimental conditions were tested: high food - low daphnid density (the optimum), low food - low daphnid density and high food - high daphnid density. In the two first conditions, daphnids experienced the same population density but they had different food availability. In the two latter conditions, daphnids had the same per capita, low, food availability but they lived at different algae and daphnid densities. Moreover, the response of crowded females to recovery at high food availability and low population density was evaluated. Low food availability reduced growth and fecundity of both clones and increased male production only in the Clone L. Crowding per se did not affect growth but reduced fecundity. In both clones, low food availability due to low algae density enhanced investment in offspring size and resistance to starvation. In response to food shortage either due to low algae density and to crowding, Clone P increased the investment in offspring size and starvation tolerance but reduced fecundity to a lesser extent than Clone L and did not produce males. Clone L, in response to food shortage due to crowding at high algae density, increased development time, produced more males, as at low algae density, but halved fecundity producing offspring that were not starvationtolerant. These results might reflect differences in anticipatory maternal effects between clones and suggest that neonate quality varies according to either, the environment the mother experienced and the competitive environment the neonates will cope due to their mother life strategy.