Prenatal Maternal Effects Research Articles

Females manipulate behavior of caring males via prenatal maternal effects

In species with biparental care, there is sexual conflict as each parent is under selection to minimize its personal effort by shifting as much as possible of the workload over to the other parent. Most theoretical and empirical work on the resolution of this conflict has focused on strategies used by both parents, such as negotiation. However, because females produce the eggs, this might afford females with an ability to manipulate male behavior via maternal effects that alter offspring phenotypes. To test this hypothesis, we manipulated the prenatal conditions (i.e., presence or absence of the male), performed a cross-fostering experiment, and monitored the subsequent effects of prenatal conditions on offspring and parental performance in the burying beetle Nicrophorus vespilloides We found that offspring were smaller at hatching when females laid eggs in presence of a male, suggesting that females invest less in eggs when expecting male assistance. Furthermore, broods laid in the presence of a male gained more weight during parental care, and they did so at the expense of male weight gain. Contrary to our expectations, males cared less for broods laid in the presence of a male. Our results provide experimental evidence that females can alter male behavior during breeding by adjusting maternal effects according to prenatal conditions. However, rather than increasing the male's parental effort, females appeared to suppress the male's food consumption, thereby leaving more food for their brood.

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.

Pre-, postnatal growth and maternal condition in a free ranging fallow deer population

We studied prenatal and postnatal growth rates and maternal effects in fallow deer (Dama dama) populations in free-ranging habitats in the Carpathian Basin. Data in this five-year long study were collected from pregnant females from December to the end of the hunting season (February), from newborns (May-June) and from 4–12 months-old fawns (October-June) in southwestern Hungary (Lábod region). The aims were to analyze foetal growth rate, assess the interaction between prenatal growth and maternal condition, and to examine factors influencing birth mass, and to measure fawn growth rates. During the study period foetal body mass (BM), body length (BL) and head length (HL) showed sigmoid growth. Correlations (rP) among the three features (BM, BL and HL) ranged from 0.78 to 0.93. Foetal BM was a quadratic function of foetal BL in both sexes. Foetal BM was linearly and negatively related to maternal kidney-fat-index (KFI) and body mass. Average birth mass was greater in males (4.66 kg) than females (4.31 kg), and it was greater in the middle of the fawning season (in the middle of June) than in the beginning (in May). The BM and the KFI of the fawns decreased at the end of the winter (February, eight months of age) but increased thereafter. The growth analysis of fawns generally showed that males compared with the females were heavier and larger; however it was not manifested clearly in all cases.

Flood‐related Prenatal Maternal Stress effects Childhood Anxiety Symptomatology; The QF2011 Queensland Flood Study

Flood‐related Prenatal Maternal Stress effects Childhood Anxiety Symptomatology; The QF2011 Queensland Flood Study

Nest-box temperature affects clutch size, incubation initiation, and nestling health in great tits

Prenatal maternal effects can be a source of phenotypic plasticity and may play a role in adaptation to climate change. However, we do not know how far temperature could influence such effects, if at all. We studied the influence of temperature during egg laying on maternal reproductive investment and on the phenotype of adult females, adult males, and nestlings. We expected temperature to have an effect, as it influences maintenance costs for females, who can also use it as a cue of the advancement of the breeding season. We experimentally increased night-time nest-box temperatures by approximately 1 °C throughout the entire laying period in great tits (Parus major). Clutch size was negatively correlated with laying date in heated females. Heated females did not delay incubation after clutch completion as frequently as control females did. Finally, blood sedimentation rate, which is an indicator of acute infections and inflammatory diseases, was positively correlated with hatching date in control broods. This suggests that nestlings were of lower quality in late-hatched broods than in early-hatched broods. This seasonal effect was not detected in heated nests. Our results show that a small increase in temperature during laying can influence breeding strategy and nestling characteristics. These results suggest that birds used temperature as a cue of seasonal advancement to adjust breeding phenology, with beneficial effects on nestling health. To better understand the consequences of maternal adjustments during egg laying, it would be interesting to combine studies with heating treatment during different periods of the breeding cycle.

Age‐related prenatal maternal effects and postnatal breeding experience have different influences on nestling development in an altricial passerine

Reproductive success and nestling performance are related to the age of parents across several vertebrate taxa. However, because breeding experience and prenatal maternal investment in reproduction often covary, the source of these age‐related differences can be difficult to determine. In this study, we evaluated the influence of prenatal maternal effects and postnatal breeding experience on the performance of nestling tree swallows Tachycineta bicolor by conducting a carefully controlled partial cross‐fostering experiment. We swapped half‐broods of nestlings between the nest of a young first‐time breeding female and the nest of a female known to have previously raised and fledged young. Our manipulation did not influence the within‐brood nestling hierarchies, and controlled for the effects of egg laying order. We found that nestlings of older females were heavier just prior to fledging regardless of the breeding experience of the attending female. In addition, fledglings raised by experienced females grew their flight feathers faster, and had greater probability of fledging. Our study demonstrates that prenatal investment in reproduction by older females can have long‐term consequences on nestling mass, and suggests limited potential for compensatory mass gains prior to fledging. Because our analyses controlled for feeding rates, our results also suggest that foraging quantity and quality are not the only benefits nestlings gain by being raised by an experienced female.

Coadaptation of offspring begging and parental provisioning: A role for prenatal maternal effects?

Recent studies on birds have shown that offspring begging and parental provisioning covary at the phenotypic level, which is thought to reflect genetic correlations. However, prenatal maternal factors, like yolk testosterone, may also facilitate parent-offspring coadaptation via their effects on offspring begging and development. In fact, maternal effects are thought to adjust offspring phenotype to the environmental conditions they will experience after birth, which are in turn strongly dependent on the levels of parental provisioning. Using cross-fostering experiments in canaries, we tested the role of maternal effects on parent-offspring coadaptation from two different approaches. First, we analyzed whether females deposit yolk testosterone in relation to their own or their partner's prospective parental provisioning, measured as the rate of parental feeding to foster nestlings. Second, we investigated whether females deposit yolk testosterone in relation to costs they incurred when raising a previous brood, as this likely impinges on their capacity to provide parental care in the near future. However, from the results of both experiments we have no evidence that canary females deposit yolk testosterone in order to match offspring begging to the levels of care they and/or their partners provide. We therefore found no evidence that yolk testosterone facilitates parent-offspring coadaptation. In addition, our results suggest that the functional consequences of yolk testosterone deposition may relate to hatching asynchrony since it primarily varied with egg laying order.

Disentangling Genetic and Prenatal Maternal Effects on Offspring Size and Survival.

Organizational processes during prenatal development can have long-term effects on an individual's phenotype. Because these early developmental stages are sensitive to environmental influences, mothers are in a unique position to alter their offspring's phenotype by differentially allocating resources to their developing young. However, such prenatal maternal effects are difficult to disentangle from other forms of parental care, additive genetic effects, and/or other forms of maternal inheritance, hampering our understanding of their evolutionary consequences. Here we used divergent selection lines for high and low prenatal maternal investment and their reciprocal line crosses in a precocial bird-the Japanese quail (Coturnix japonica)-to quantify the relative importance of genes and prenatal maternal effects in shaping offspring phenotype. Maternal but not paternal origin strongly affected offspring body size and survival throughout development. Although the effects of maternal egg investment faded over time, they were large at key life stages. Additionally, there was evidence for other forms of maternal inheritance affecting offspring phenotype at later stages of development. Our study is among the first to successfully disentangle prenatal maternal effects from all other sources of confounding variation and highlights the important role of prenatal maternal provisioning in shaping offspring traits closely linked to fitness.

A loss of heterozygosity, a loss in competition? The effects of inbreeding, pre- and postnatal conditions on nestling development.

The early developmental trajectory is affected by genetic and environmental factors that co‐depend and interact often in a complex way. In order to distinguish their respective roles, we used canaries (Serinus canaria) of different genetic backgrounds (inbred and outbred birds). An artificial size hierarchy was created to provoke within‐nest competition, manipulating postnatal conditions. To this end, inbred birds were weight‐matched with outbred birds into duos, and each nest contained one duo of size‐advantaged, and one duo of size‐disadvantaged inbred and outbred nestlings. Prenatal (maternal) effects were taken into account also, enabling us to study the separate as well as the interactive effects of inbreeding, pre‐ and postnatal conditions on nestling development. We find that postnatal conditions were the most important determinant of early growth, with size‐advantaged nestlings growing faster and obtaining larger size/body mass at fledging in comparison with size‐disadvantaged nestlings. Prenatal conditions were important too, with birds that hatched from eggs that were laid late in the laying order obtaining a larger size at fledging than those hatched from early laid eggs. Inbreeding inhibited growth, but surprisingly this did not depend on (dis)advantageous pre‐ or postnatal conditions. Our findings imply that inbred individuals lose when they are in direct competition with same‐sized outbred individuals regardless of the rearing conditions, and we thus propose that reduced competitiveness is one of the driving forces of inbreeding depression.

Matrilineal inheritance of a key mediator of prenatal maternal effects.

Sex-linkage is predicted to evolve in response to sex-specific or sexually antagonistic selection. In line with this prediction, most sex-linked genes are associated with reproduction in the respective sex. In addition to traits directly involved in fertility and fecundity, mediators of maternal effects may be predisposed to evolve sex-linkage, because they indirectly affect female fitness through their effect on offspring phenotype. Here, we test for sex-linked inheritance of a key mediator of prenatal maternal effects in oviparous species, the transfer of maternally derived testosterone to the eggs. Consistent with maternal inheritance, we found that in Japanese quail (Coturnix japonica) granddaughters resemble their maternal (but not their paternal) grandmother in yolk testosterone deposition. This pattern of resemblance was not due to non-genetic priming effects of testosterone exposure during prenatal development, as an experimental manipulation of yolk testosterone levels did not affect the females' testosterone transfer to their own eggs later in life. Instead, W chromosome and/or mitochondrial variation may underlie the observed matrilineal inheritance pattern. Ultimately, the inheritance of mediators of maternal effects along the maternal line will allow for a fast and direct response to female-specific selection, thereby affecting the dynamics of evolutionary processes mediated by maternal effects.

High Yolk Testosterone Transfer Is Associated with an Increased Female Metabolic Rate.

Yolk androgens of maternal origin are important mediators of prenatal maternal effects. Although in many species short-term benefits of exposure to high yolk androgen concentrations for the offspring have been observed, females differ substantially in the amount of androgens they transfer to their eggs. It suggests that costs for the offspring or the mother constrain the evolution of maternal hormone transfer. However, to date, the nature of these costs remains poorly understood. Unlike most previous work that focused on potential costs for the offspring, we here investigated whether high yolk testosterone transfer is associated with metabolic costs (i.e., a higher metabolic rate) for the mother. We show that Japanese quail (Coturnix japonica) females that deposit higher testosterone concentrations into their eggs have a higher resting metabolic rate. Because a higher metabolic rate is often associated with a shorter life span, this relationship may explain the negative association between yolk testosterone transfer and female longevity observed in the wild. Our results suggest that metabolic costs for the mother can balance the short-term benefits of yolk testosterone exposure for the offspring, thereby contributing to the maintenance of variation in maternal yolk hormone transfer in natural populations.

In search of genetic constraints limiting the evolution of egg size: direct and correlated responses to artificial selection on a prenatal maternal effector.

Maternal effects are an important force in nature, but the evolutionary dynamics of the traits that cause them are not well understood. Egg size is known to be a key mediator of prenatal maternal effects with an established genetic basis. In contrast to theoretical expectations for fitness-related traits, there is a large amount of additive genetic variation in egg size observed in natural populations. One possible mechanism for the maintenance of this variation is through genetic constraints caused by a shared genetic basis among traits. Here we created replicated, divergent selection lines for maternal egg investment in Japanese quail (Coturnix japonica) to quantify the role of genetic constraints in the evolution of egg size. We found that egg size responds rapidly to selection, accompanied by a strong response in all egg components. Initially, we observed a correlated response in body size, but this response declined over time, showing that egg size and body size can evolve independently. Furthermore, no correlated response in fecundity (measured as the proportion of days on which a female laid an egg) was observed. However, the response to selection was asymmetrical, with egg size plateauing after one generation of selection in the high but not the low investment lines. We attribute this pattern to the presence of genetic asymmetries, caused by directional dominance or unequal allele frequencies. Such asymmetries may contribute to the evolutionary stasis in egg size observed in natural populations, despite a positive association between egg size and fitness.

Differential Effects of Maternal Yolk Androgens on Male and Female Offspring: A Role for Sex-Specific Selection?

Maternal hormones are important mediators of prenatal maternal effects in animals. Although their effects on offspring phenotype are often sex-specific, the reason why sometimes sons are more sensitive to prenatal hormone exposure and sometimes daughters is not well understood. Here I combine an experimental manipulation of yolk testosterone concentration in the egg and quantification of selection acting on yolk androgen-sensitive traits in a natural population of great tits (Parus major) with a literature review to test the hypothesis that sex-specific selection on traits affected by yolk androgens determines which sex is more sensitive to prenatal hormone exposure. An experimental increase of the testosterone content in the egg boosted the post-hatching growth of male, but not female great tit nestlings. However, I found no evidence that survival selection on body mass or size is acting differently in the two sexes. A literature review revealed that yolk androgen manipulations affect the growth of males and females differently across species. Interestingly, in studies performed in the wild a significant association between the strength and direction of sexual size dimorphism and sex-specific sensitivities to yolk androgens was observed. In studies performed in captivity, no such relationship was found. Thus, across species there is some evidence that sex-specific selection on body size influences how strongly growth trajectories of males and females are affected by maternally-derived yolk androgens.

Combining information from ancestors and personal experiences to predict individual differences in developmental trajectories.

A persistent question in biology is how information from ancestors combines with personal experiences over the lifetime to affect the developmental trajectories of phenotypic traits. We address this question by modeling individual differences in behavioral developmental trajectories on the basis of two assumptions: (1) differences among individuals in the behavior expressed at birth or hatching are based on information from their ancestors (via genes, epigenes, and prenatal maternal effects), and (2) information from ancestors is combined with information from personal experiences over ontogeny via Bayesian updating. The model predicts relationships between the means and the variability of the behavior expressed by neonates and the subsequent developmental trajectories of their behavior when every individual is reared under the same environmental conditions. Several predictions of the model are supported by data from previous studies of behavioral development, for example, that the temporal stability of personality will increase with age and that the intercepts and slopes of developmental trajectories for boldness will be negatively correlated across individuals or genotypes when subjects are raised in safe environments. We describe how other specific predictions of the model can be used to test the hypothesis that information from ancestors and information from personal experiences are combined via nonadditive, Bayesian-like processes.

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.

Prenatal Maternal and Possible Transgenerational Epigenetic Effects on Milk Production

This study investigated whether the prenatal maternal environment in dairy cattle influences the postnatal milking performance of the resulting daughters and grand-daughters. Linear mixed models were used to analyse whole season milk production from ∼46000 Jersey and ∼123000 Holstein Friesian cows in their 1st and 2nd lactations. Variation in the prenatal environment was associated with a small but significant (P<0.05) proportion of the total phenotypic variation (0.010 to 0.015) in all traits in Holstein Friesian cows and in the first lactation milk volume (0.011) and milk protein (0.011), and the second lactation milk fat (0.015) in the Jersey breed. This indicates that the prenatal environment does influence the adult performance of the subsequent daughter. Associations between daughter performance and dam and grand-dam traits indicative of their prenatal environment were also estimated. A one litre increase in the dam’s herd test milk volume was associated with a 7.5 litre increase in the daughters’ whole season milk yield and a 1% increase in either the dams’ herd test milk fat or protein percentage was associated with a reduction in daughter whole season milk volume (−49.6 and −45.0 litres for dam fat and protein, respectively). Similar results between the grand-dam herd test traits ansd the daughters’ whole season milk production were observed with a 1% increase in either grand-dam milk fat or protein percentage associated with a reduction in daughter whole season milk yield (−34.7 and −9.7 litres for fat and protein, respectively). This study revealed that the prenatal environment of the dam and the grand-dam can influence milk production in the subsequent daughters, though the effects are small. The similarity of the results between the dam daughter and the grand-dam daughter analyses suggests that the majority of the prenatal maternal effects are mediated by epigenetic mechanisms.

Long‐term effects of litter sex ratio on female reproduction in two iteroparous mammals

Summary Female mammals that develop in male‐biased litters show signs of masculinization because they are exposed to the testosterone produced by their male siblings in utero. The early exposure to testosterone can affect female morphology, physiology, behaviour and life‐history traits. Masculinization is commonly seen as the collateral effect of developing in a male‐biased litter. However, when resources are limiting, masculinization might be adaptive because androgenized females could monopolize resources. We investigated whether females from male‐biased litters, and therefore likely to be masculinized, showed adaptive advantages under different competing scenarios. For that, we used data from two long‐term field projects studying yellow‐bellied marmots (Marmota flaviventris Audubon and Bachman, 1841) and European rabbits (Oryctolagus cuniculus Linnaeus, 1758). We explored whether litter sex composition affected fitness‐related reproductive traits: the onset of breeding, offspring production and the probability of reproduction in a given year. Our study shows long‐term consequences of litter sex composition on reproduction in European rabbits and yellow‐bellied marmots. Females from male‐biased litters from both species delayed the onset of breeding, suggesting the maladaptive nature of masculinization. However, in European rabbits, this effect was density‐dependent. Under higher‐density conditions, female rabbits from male‐biased litters brought forward the onset of breeding, which might increase the probability of offspring overwinter survival and therefore their fitness. These females under limiting conditions might have a higher resource holding potential. We conclude that prenatal maternal effects in natural populations should be taken into account when studying life‐history variation. Moreover, it is notable that small variations in naturally occurring prenatal exposure to androgens have profound impacts on individuals, social groups and the population structure.

Interactions between prenatal maternal effects and posthatching conditions in a wild bird population

Resources and cues provided by the mother before birth are important mediators of developmental plasticity. It has been suggested that the adaptive value of such prenatal maternal effects may depend on the environment encountered by the offspring after birth, and that offspring may perform better when environmental conditions encountered by the mother and the offspring match, than when a mismatch occurs. Here, we test how prenatal maternal effects and postnatal conditions interact in influencing offspring growth and development in wild-living great tits (Parus major) by manipulating food availability experienced by the mother before egg laying, partially cross-fostering nestlings between nests, and manipulating food availability after hatching. We observed significant interaction effects between pre- and postnatal food conditions. Nonsupplemented nestlings reached a similar fledging mass, a trait closely linked to postfledging survival, as food-supplemented nestlings when their biological mother had received extra food during egg laying. It shows that prenatal maternal investment can compensate for growth-limiting conditions after hatching. This effect was sex specific, with daughters benefiting more than sons. Furthermore, food-supplemented nestlings grew largest when their biological mother had not received extra food during egg laying, suggesting that offspring were primed prenatally, possibly through differential egg composition, to use resources more efficiently. However, we found no evidence that offspring performed generally better when pre- and postnatal food conditions matched than when a mismatch occurred. Our results demonstrate the importance of considering the postnatal environment when testing for the ecological and evolutionary consequences of prenatal maternal effects in natural populations.Resources transferred by the bird mother via the egg help to reduce the negative consequences of a harsh environment after birth. Furthermore, mothers encountering harsh environmental conditions during egg laying prime their offspring to use available resources more efficiently later in life. Our study shows that the environment encountered before birth can have important long-term consequences on offspring performance and the way animals interact with their environment.

The multivariate egg: quantifying within- and among-clutch correlations between maternally derived yolk immunoglobulins and yolk androgens using multivariate mixed models

Egg components are important mediators of prenatal maternal effects in birds and other oviparous species. Because different egg components can have opposite effects on offspring phenotype, selection is expected to favour their mutual adjustment, resulting in a significant covariation between egg components within and/or among clutches. Here we tested for such correlations between maternally derived yolk immunoglobulins and yolk androgens in great tit (Parus major) eggs using a multivariate mixed-model approach. We found no association between yolk immunoglobulins and yolk androgens within clutches, indicating that within clutches the two egg components are deposited independently. Across clutches, however, there was a significant negative relationship between yolk immunoglobulins and yolk androgens, suggesting that selection has co-adjusted their deposition. Furthermore, an experimental manipulation of ectoparasite load affected patterns of covariance among egg components. Yolk immunoglobulins are known to play an important role in nestling immune defence shortly after hatching, whereas yolk androgens, although having growth-enhancing effects under many environmental conditions, can be immunosuppressive. We therefore speculate that variation in the risk of parasitism may play an important role in shaping optimal egg composition and may lead to the observed pattern of yolk immunoglobulin and yolk androgen deposition across clutches. More generally, our case study exemplifies how multivariate mixed-model methodology presents a flexible tool to not only quantify, but also test patterns of (co)variation across different organisational levels and environments, allowing for powerful hypothesis testing in ecophysiology.

Bigger mothers are better mothers: disentangling size-related prenatal and postnatal maternal effects

Despite a vast literature on the factors controlling adult size, few studies have investigated how maternal size affects offspring size independent of direct genetic effects, thereby separating prenatal from postnatal influences. I used a novel experimental design that combined a cross-fostering approach with phenotypic manipulation of maternal body size that allowed me to disentangle prenatal and postnatal maternal effects. Using the burying beetle Nicrophorus vespilloides as model organism, I found that a mother's body size affected egg size as well as the quality of postnatal maternal care, with larger mothers producing larger eggs and raising larger offspring than smaller females. However, with respect to the relative importance of prenatal and postnatal maternal effects on offspring growth, only the postnatal effects were important in determining offspring body size. Thus, prenatal effects can be offset by the quality of postnatal maternal care. This finding has implications for the coevolution of prenatal and postnatal maternal effects as they arise as a consequence of maternal body size. In general, my study provides evidence that there can be transgenerational phenotypic plasticity, with maternal size determining offspring size leading to a resemblance between mothers and their offspring above and beyond any direct genetic effects.