Maternal food quantity affects offspring feeding rate in Daphnia magna

Maternal effects have wide-ranging effects on life-history traits. Here, using the crustacean Daphnia magna, we document a new effect: maternal food quantity affects offspring feeding rate, with low quantities of food triggering mothers to produce slow-feeding offspring. Such a change in the rate of resource acquisition has broad implications for population growth or dynamics and for interactions with, for instance, predators and parasites. This maternal effect can also explain the previously puzzling situation that the offspring of well-fed mothers, despite being smaller, grow and reproduce better than the offspring of food-starved mothers. As an additional source of variation in resource acquisition, this maternal effect may also influence relationships between life-history traits, i.e. trade-offs, and thus constraints on adaptation. Maternal nutrition has long-lasting effects on health and particularly diet-related traits in humans; finding an effect of maternal nutrition on offspring feeding rate in Daphnia highlights the utility of this organism as a powerful experimental model for exploring the relationship between maternal diet and offspring fitness.     

Genetic variation for maternal effects on parasite susceptibility

The expression of infectious disease is increasingly recognized to be impacted by maternal effects, where the environmental conditions experienced by mothers alter resistance to infection in offspring, independent of heritability. Here, we studied how maternal effects (high or low food availability to mothers) mediated the resistance of the crustacean Daphnia magna to its bacterial parasite Pasteuria ramosa. We sought to disentangle maternal effects from the effects of host genetic background by studying how maternal effects varied across 24 host genotypes sampled from a natural population. Under low‐food conditions, females produced offspring that were relatively resistant, but this maternal effect varied strikingly between host genotypes, i.e. there were genotype by maternal environment interactions. As infection with P. ramosa causes a substantial reduction in host fecundity, this maternal effect had a large effect on host fitness. Maternal effects were also shown to impact parasite fitness, both because they prevented the establishment of the parasites and because even when parasites did establish in the offspring of poorly fed mothers, and they tended to grow more slowly. These effects indicate that food stress in the maternal generation can greatly influence parasite susceptibility and thus perhaps the evolution and coevolution of host–parasite interactions.     

Testing hypotheses for maternal effects in Daphnia magna

Maternal effects are widely observed, but their adaptive nature remains difficult to describe and interpret. We investigated adaptive maternal effects in a clone of the crustacean Daphnia magna, experimentally varying both maternal age and maternal food and subsequently varying food available to offspring. We had two main predictions: that offspring in a food environment matched to their mothers should fare better than offspring in unmatched environments, and that offspring of older mothers would fare better in low food environments. We detected numerous maternal effects, for example offspring of poorly fed mothers were large, whereas offspring of older mothers were both large and showed an earlier age at first reproduction. However, these maternal effects did not clearly translate into the predicted differences in reproduction. Thus, our predictions about adaptive maternal effects in response to food variation were not met in this genotype of Daphnia magna.     

Implications of maternal nutrient restriction in transgenerational programming of hypertension and endothelial dysfunction across F1-F3 offspring

AimsAn extensive variety of prenatal insults are associated with an increased incidence of metabolic and cardiovascular disorders in adult life. We previously demonstrated that maternal global nutrient restriction during pregnancy leads to increased blood pressure and endothelial dysfunction in the adult offspring. This study aimed to assess whether prenatal exposure to nutritional insult has transgenerational effects in F₂ and F₃ offspring.Main methodsFor this, female Wistar rats were randomly divided into two groups on day 1 of pregnancy: a control group fed standard chow ad libitum and a restricted group fed 50% of the ad libitum intake throughout gestation. At delivery, all animals were fed a standard laboratory chow diet. At 11 weeks of age, one female and one male from each restricted litter were randomly selected and mated with rats from another restricted litters in order to generate the F₂ offspring. The same procedure produced F₃ generation. Similarly, the rats in the control group were bred for each generation.Key FindingsOur findings show that the deleterious effects of maternal nutrient restriction to which the F₀ mothers were exposed may not be limited to the male first generation. In fact, we found that elevated blood pressure, an impaired vasodilatory response to acetylcholine and alterations in NO production were all transferred to the subsequent males from F₂ and F₃ generations.SignificanceOur data show that global nutrient restriction during pregnancy results in a specific phenotype that can be passed transgenerationally to a second and third generation.     

Family planning inDaphnia: resistance to starvation in offspring born to mothers grown at different food levels

Summary We observed a shift in maternal investment per offspring in clonal cultures of twoDaphnia species. Mothers grown at high food levels produced large clutches of smaller eggs but their offspring could not survive long under starvation conditions. Genetically identical mothers grown at low food levels produced small cultches of larger eggs, and their offspring, albeit low in numbers, were able to survive long periods of starvation. Our data show thatDaphnia mothers are capable of assessing food level and use this information in adjusting their fractional peroffspring allocation of reproductive resources.     

Transgenerational effects of poor elemental food quality on Daphnia magna

Environmental effects on parents can strongly affect the phenotype of their offspring, which alters the heritability of traits and the offspring’s responses to the environment. We examined whether P limitation of the aquatic invertebrate, Daphnia magna, alters the responses of its offspring to inadequate P nutrition. Mother Daphnia consuming P-poor algal food produced smaller neonates having lower body P content compared to control (P-rich) mothers. These offspring from P-stressed mothers, when fed P-rich food, grew faster and reproduced on the same schedule as those from P-sufficient mothers. In contrast, offspring from P-stressed mothers, when fed P-poor food, grew more slowly and had delayed reproduction compared to their sisters born to control mothers. There was also weak evidence that daughters from P-stressed mothers are more susceptible to infection by the virulent bacterium, Pasteuria ramosa. Our results show that P stress is not only transferred across generations, but also that its effect on the offspring generation varies depending upon the quality of their own environment. Maternal P nutrition can thus determine the nature of offspring responses to food P content and potentially obfuscates relationships between the performance of offspring and their own nutrition. Given that food quality can be highly variable within and among natural environments, our results demonstrate that maternal effects should be included as an additional dimension into studies of how elemental nutrition affects the physiology, ecology, and evolution of animal consumers.     

Cross-generational environmental effects and the evolution of offspring size in the Trinidadian guppy Poecilia reticulata

Abstract The existence of adaptive phenotypic plasticity demands that we study the evolution of reaction norms, rather than just the evolution of fixed traits. This approach requires the examination of functional relationships among traits not only in a single environment but across environments and between traits and plasticity itself. In this study, I examined the interplay of plasticity and local adaptation of offspring size in the Trinidadian guppy, Poecilia reticulata. Guppies respond to food restriction by growing and reproducing less but also by producing larger offspring. This plastic difference in offspring size is of the same order of magnitude as evolved genetic differences among populations. Larger offspring sizes are thought to have evolved as an adaptation to the competitive environment faced by newborn guppies in some environments. If plastic responses to maternal food limitation can achieve the same fitness benefit, then why has guppy offspring size evolved at all? To explore this question, I examined the plastic response to food level of females from two natural populations that experience different selective environments. My goals were to examine whether the plastic responses to food level varied between populations, test the consequences of maternal manipulation of offspring size for offspring fitness, and assess whether costs of plasticity exist that could account for the evolution of mean offspring size across populations. In each population, full‐sib sisters were exposed to either a low‐ or high‐food treatment. Females from both populations produced larger, leaner offspring in response to food limitation. However, the population that was thought to have a history of selection for larger offspring was less plastic in its investment per offspring in response to maternal mass, maternal food level, and fecundity than the population under selection for small offspring size. To test the consequences of maternal manipulation of offspring size for offspring fitness, I raised the offspring of low‐ and high‐food mothers in either low‐ or high‐food environments. No maternal effects were detected at high food levels, supporting the prediction that mothers should increase fecundity rather than offspring size in noncompetitive environments. For offspring raised under low food levels, maternal effects on juvenile size and male size at maturity varied significantly between populations, reflecting their initial differences in maternal manipulation of offspring size; nevertheless, in both populations, increased investment per offspring increased offspring fitness. Several correlates of plasticity in investment per offspring that could affect the evolution of offspring size in guppies were identified. Under low‐food conditions, mothers from more plastic families invested more in future reproduction and less in their own soma. Similarly, offspring from more plastic families were smaller as juveniles and female offspring reproduced earlier. These correlations suggest that a fixed, high level of investment per offspring might be favored over a plastic response in a chronically low‐resource environment or in an environment that selects for lower reproductive effort     

Intrauterine growth restriction affects bone mineral density of the mandible and the condyle in growing rats

Objectives:To investigate in growing rats the effect of intrauterine growth restriction (IUGR) on the bone mineral density of the mandible and tibia, as well as the quality of the mandibular and condylar bone.Methods:Twelve male rats were born IUGR by mothers sustaining 50% food restriction during pregnancy. Twelve control male rats were born by mothers fed ad libitum. Dual-energy X-ray absorptiometry (DEXA) of the tibia, proximal tibial metaphysis and the mandible, biochemical markers, histology and histomorphometrical analysis on the mandibular and subchondral bone of the condyle were performed.Results:IUGR significantly affected bone mineral density (BMD) of both tibial and mandibular bones. IUGR rats had significantly lower osteocalcin values (p=0.021) and phosphorus (p=0.028), but not 25-OH vitamin D (p=0.352). Bone area percentage in the mandible was significantly lower (51.21±5.54) in IUGR compared to controls (66.00±15.49), and for subchondral bone of the condyle for IUGR (47.01±6.82) compared to controls (68.27±13.37). IUGR had a significant reduction in the fibrous layer, but not the proliferating layer, with the hypertrophic layer significantly increased.Conclusion:Maternal restricted nutrition during gestation can affect BMD of the mandible and the tibia of the offspring animals.     

Food availability modulates the effects of maternal antibodies on growth and immunity in young feral pigeons

It is now widely acknowledged that mothers can transfer their own immune experience to their progeny through the allocation of specific maternal antibodies (hereafter referred as MatAb) that can shape offspring phenotype and affect their fitness. However, the importance of environmental variability in modulating the effects of MatAb on offspring traits is still elusive. Using an experimental approach, we investigated how food availability interacted with MatAb to solve the trade‐off between humoral immunity and growth in young feral pigeons Columba livia. Results show that the inhibitory effect of MatAb on the humoral response of chicks was detected regardless of the food treatment. In addition, body mass growth was higher in chicks receiving lower amounts of maternal antibodies but only in chicks of the ad libitum food treatment. This contradicts previous studies and suggests that the transfer of MatAb could entail some costs for chicks and reduce their growth. Taken together these results reinforce the idea that the maternal antibodies play a central role in shaping offspring life‐history traits but that their adaptive value is highly dependent on the environmental context in which they are transmitted by the mother.     

Life-History Characteristics and Fitness in Descendents of Parthenogenetic and Ex-Ephippio Females of Daphnia Magna

Daphnids of ex-ephippial and parthenogenetic origin differ substantially in life-history. Possible maternally transmitted ex-diapause effects of differing female origin on the fitness of their offspring were studied across multiple clones in Daphnia magna. Ex-ephippial daphnids responded in egg size to different constant food concentrations with the same pattern as parthenogenetic females. Significant differences in egg characteristics between females of different origin were only found for the first clutch produced under high food. The smaller size of eggs in ex-ephippial females, however, did not translate into size differences of first-clutch neonates. A trend for lower mass density per body volume was detected in offspring from ex-ephippial females in comparison with parthenogenetic daphnids. Hence, an ex-diapause effect transmitted by ex-ephippial mothers to their parthenogenetic offspring is likely. However, there was no difference in life-histories and fitness between offspring produced by females of ex-ephippial and parthenogenetic origin at both, high and low food concentrations across multiple clones. Thus, a significant ex-diapause effect on fitness in successive parthenogenetic generations may not be expected in D. magna at the population level.     

Older mothers follow conservative strategies under predator pressure: The adaptive role of maternal glucocorticoids in yellow-bellied marmots

When the maternal environment is a good predictor of the offspring environment, maternal glucocorticoid (GC) levels might serve to pre-program offspring to express certain phenotypes or life-history characteristics that will increase their fitness. We conducted a field study to assess the effects of naturally occurring maternal GC levels on their offspring in yellow-bellied marmots (Marmota flaviventris) subjected to different predator pressures. Maternal fecal corticosteroid metabolites (FCM) were positively correlated with predator pressure. Predators had both direct and indirect effects on pups. We found that older mothers with higher FCM levels had smaller and female-biased litters. Moreover, sons from older mothers with high FCM levels dispersed significantly more than those from older mothers with low FCM levels, whereas the opposite pattern was found in pups from younger mothers. These age-related effects may permit females to make adaptive decisions that increase their pups' fitness according to their current situation.     

Direct and trans-generational responses to food deprivation during development in the Glanville fritillary butterfly

Life history characteristics and resulting fitness consequences manifest not only in an individual experiencing environmental conditions but also in its offspring via trans-generational effects. We conducted a set of experiments to assess the direct and trans-generational effects of food deprivation in the Glanville fritillary butterfly Melitaea cinxia. Food availability was manipulated during the final stages of larval development and performance was assessed during two generations. Direct responses to food deprivation were relatively minor. Food-deprived individuals compensated, via increased development time, to reach a similar mass as adults from the control group. Delayed costs of compensatory growth were observed, as food-deprived individuals had either reduced fecundity or lifespan depending on the type of feeding treatment they had experienced (intermittent vs. continuous). Female food deprivation did not directly affect her offspring’s developmental trajectory, but the way the offspring coped with food deprivation. Offspring of mothers from control or intermittent starvation treatments reached the size of those in the control group via increased development time when being starved. In contrast, offspring of mothers that had experienced 2 days of continuous food deprivation grew even larger than control animals, when deprived of food themselves. Offspring of food-deprived Glanville fritillary initially showed poor immune response to parasitism, but not later on in development.     

Effect of match or mismatch of maternal-offspring nutritional environment on the development of offspring in broiler chickens

In mammals, maternal food restriction around conception and during pregnancy results in low birth weight and an adjusted growth trajectory of offspring. If, subsequently, the offspring are born into a food-abundant environment, they are at increased risk of developing obesity, type 2 diabetes, hypertension and renal dysfunction. Here, we show similar effects of maternal undernutrition on hatch weight, growth and fat deposition in offspring of birds (domestic chicken). Both mothers and offspring were fed either ad libitum or restricted in a two-by-two factorial design, resulting in two matched and two mismatched maternal-offspring nutritional environments. Offspring of ad libitum mothers grew heavier than those of restricted mothers, possibly due to the larger muscle mass. Ad libitum-fed offspring, especially females, of restricted mothers were lighter at hatch, and were heavier and had more abdominal fat at 6 weeks of age than daughters of ad libitum-fed mothers. These results suggest a common mechanism in mammals and birds in response to a mismatch in the maternal-offspring nutritional environment. They also indicate that the common practice of restrictive feeding of the broiler breeders and subsequent ad libitum feeding of the broilers may result in reduced growth and increased abdominal fat as compared to broilers of less restricted broiler breeders.     

Involvement of the GHSR in the developmental programming and metabolic disturbances induced by maternal undernutrition

The mismatch between maternal undernutrition and adequate nutrition after birth increases the risk of developing metabolic diseases. We aimed to investigate whether the hyperghrelinemia during maternal undernourishment rewires the hypothalamic development of the offspring and contributes to the conversion to an obese phenotype when fed a high-fat diet (HFD). Pregnant C57BL/6 J, wild type (WT) and ghrelin receptor (GHSR)^−/− mice were assigned to either a normal nourished (NN) group, or an undernutrition (UN) (30% food restricted) group. All pups were fostered by NN Swiss mice. After weaning, pups were fed a normal diet, followed by a HFD from week 9. Plasma ghrelin levels peaked at postnatal day 15 (P15) in both C57BL/6 J UN and NN pups. Hypothalamic Ghsr mRNA expression was upregulated at P15 in UN pups compared to NN pups and inhibited agouti-related peptide (AgRP) projections. Adequate lactation increased body weight of UN WT but not of GHSR^−/− pups compared to NN littermates. After weaning with a HFD, body weight and food intake was higher in WT UN pups but lower in GHSR^−/− UN pups than in NN controls. The GHSR prevented a decrease in ambulatory activity and oxygen consumption in UN offspring during ad libitum feeding. Maternal undernutrition triggers developmental changes in the hypothalamus in utero which were further affected by adequate feeding after birth during the postnatal period by affecting GHSR signaling. The GHSR contributes to the hyperphagia and the increase in body weight when maternal undernutrition is followed by an obesity prone life environment.     

Bigger is better: changes in body size explain a maternal effect of food on offspring disease resistance

Maternal effects triggered by changes in the environment (e.g., nutrition or crowding) can influence the outcome of offspring–parasite interactions, with fitness consequences for the host and parasite. Outside of the classic example of antibody transfer in vertebrates, proximate mechanisms have been little studied, and thus, the adaptive significance of maternal effects on infection is not well resolved. We sought to determine why food‐stressed mothers give birth to offspring that show a low rate of infection when the crustacean Daphnia magna is exposed to an orally infective bacterial pathogen. These more‐resistant offspring are also larger at birth and feed at a lower rate. Thus, reduced disease resistance could result from slow‐feeding offspring ingesting fewer bacterial spores or because their larger size allows for greater immune investment. To distinguish between these theories, we performed an experiment in which we measured body size, feeding rate, and susceptibility, and were able to show that body size is the primary mechanism causing altered susceptibility: Larger Daphnia were less likely to become infected. Contrary to our predictions, there was also a trend that fast‐feeding Daphnia were less likely to become infected. Thus, our results explain how a maternal environmental effect can alter offspring disease resistance (though body size), and highlight the potential complexity of relationship between feeding rate and susceptibility in a host that encounters a parasite whilst feeding.     

Maternal caloric restriction partially rescues the deleterious effects of advanced maternal age on offspring

While many studies have focused on the detrimental effects of advanced maternal age and harmful prenatal environments on progeny, little is known about the role of beneficial non‐Mendelian maternal inheritance on aging. Here, we report the effects of maternal age and maternal caloric restriction (CR) on the life span and health span of offspring for a clonal culture of the monogonont rotifer Brachionus manjavacas. Mothers on regimens of chronic CR (CCR) or intermittent fasting (IF) had increased life span compared with mothers fed ad libitum (AL). With increasing maternal age, life span and fecundity of female offspring of AL‐fed mothers decreased significantly and life span of male offspring was unchanged, whereas body size of both male and female offspring increased. Maternal CR partially rescued these effects, increasing the mean life span of AL‐fed female offspring but not male offspring and increasing the fecundity of AL‐fed female offspring compared with offspring of mothers of the same age. Both maternal CR regimens decreased male offspring body size, but only maternal IF decreased body size of female offspring, whereas maternal CCR caused a slight increase. Understanding the genetic and biochemical basis of these different maternal effects on aging may guide effective interventions to improve health span and life span.     

Daphnia magna microRNAs respond to nutritional stress and ageing but are not transgenerational

Maternal effects, where the performance of offspring is determined by the condition of their mother, are widespread and may in some cases be adaptive. The crustacean Daphnia magna shows strong maternal effects: offspring size at birth and other proxies for fitness are altered when their mothers are older or when mothers have experienced dietary restriction. The mechanisms for this transgenerational transmission of maternal experience are unknown, but could include changes in epigenetic patterning. MicroRNAs (miRNAs) are regulators of gene expression that have been shown to play roles in intergenerational information transfer, and here, we test whether miRNAs are involved in D. magna maternal effects. We found that miRNAs were differentially expressed in mothers of different ages or nutritional state. We then examined miRNA expression in their eggs, their adult daughters and great granddaughters, which did not experience any treatments. The maternal (treatment) generation exhibited differential expression of miRNAs, as did their eggs, but this was reduced in adult daughters and lost by great granddaughters. Thus, miRNAs are a component of maternal provisioning, but do not appear to be the cause of transgenerational responses under these experimental conditions. MicroRNAs may act in tandem with egg provisioning (e.g., with carbohydrates or fats), and possibly other small RNAs or epigenetic modifications.     

Short-term benefits,but transgenerational costs of maternal loss in an insect with facultative maternal care

A lack of parental care is generally assumed to entail substantial fitness costs for offspring that ultimately select for the maintenance of family life across generations. However, it is unknown whether these costs arise when parental care is facultative, thus questioning their fundamental importance in the early evolution of family life. Here, we investigated the short-term, long-term and transgenerational effects of maternal loss in the European earwig Forficula auricularia, an insect with facultative post-hatching maternal care. We showed that maternal loss did not influence the developmental time and survival rate of juveniles, but surprisingly yielded adults of larger body and forceps size, two traits associated with fitness benefits. In a cross-breeding/cross-fostering experiment, we then demonstrated that maternal loss impaired the expression of maternal care in adult offspring. Interestingly, the resulting transgenerational costs were not only mediated by the early-life experience of tending mothers, but also by inherited, parent-of-origin-specific effects expressed in juveniles. Orphaned females abandoned their juveniles for longer and fed them less than maternally-tended females, while foster mothers defended juveniles of orphaned females less well than juveniles of maternally-tended females. Overall, these findings reveal the key importance of transgenerational effects in the early evolution of family life.     

Food quantity and quality shapes reproductive strategies of Daphnia

In freshwater environments, one of the challenges aquatic grazers face are periods of suboptimal food quantity and quality. In a life table experiment, the effects of food quantity (a gradient of algae concentration) and quality (a diet of cyanobacteria) on the life histories and resource allocation strategy in Daphnia magna were tested. Growth‐related traits were similarly affected under different food regimes while the reproductive strategies differed in animals exposed to low food quantity and quality. The per‐clutch investment (clutch volume) did not differ between Daphnia fed with cyanobacteria and underfed mothers, but resources were differently allocated; underfed mothers increased their per‐offspring investment by producing fewer, but larger eggs, whereas cyanobacteria‐fed mothers invested in a greater number of eggs of smaller size. I argue that both strategies of resource allocation (number vs. size of eggs) may be adaptive under the given food regime. The results of the study show that the cyanobacteria diet‐driven fitness losses are comparable to losses caused by food quantity, which is only slightly above the growth capability threshold for Daphnia.     

Maternal dietary folate and/or vitamin B12 restrictions alter body composition (adiposity) and lipid metabolism in Wistar rat offspring

Maternal vitamin deficiencies are associated with low birth weight and increased perinatal morbidity and mortality. We hypothesize that maternal folate and/or vitamin B₁₂ restrictions alter body composition and fat metabolism in the offspring. Female weaning Wistar rats received ad libitum for 12 weeks a control diet (American Institute of Nutrition-76A) or the same with restriction of folate, vitamin B₁₂ or both (dual deficient) and, after confirming vitamin deficiency, were mated with control males. The pregnant/lactating mothers and their offspring received their respective diets throughout. Biochemical and body composition parameters were determined in mothers before mating and in offspring at 3, 6, 9 and 12 months of age. Vitamin restriction increased body weight and fat and altered lipid profile in female Wistar rats, albeit differences were significant with only B₁₂ restriction. Offspring born to vitamin-B₁₂-restricted dams had lower birth weight, while offspring of all vitamin-restricted dams weighed higher at/from weaning. They had higher body fat (specially visceral fat) from 3 months and were dyslipidemic at 12 months, when they had high circulating and adipose tissue levels of tumor necrosis factor α, leptin and interleukin 6 and low levels of adiponectin and interleukin 1β. Vitamin-restricted offspring had higher activities of hepatic fatty acid synthase and acetyl-CoA-carboxylase and higher plasma cortisol levels. In conclusion, maternal and peri-/postnatal folate and/or vitamin B₁₂ restriction increased visceral adiposity (due to increased corticosteroid stress), altered lipid metabolism in rat offspring perhaps by modulating adipocyte function and may thus predispose them to high morbidity later.