Relationship between maternal environment and DNA methylation patterns of estrogen receptor alpha in wild Eastern Bluebird (Sialia sialis) nestlings: a pilot study

There is mounting evidence that, across taxa, females breeding in competitive environments tend to allocate more testosterone to their offspring prenatally and these offspring typically have more aggressive and faster‐growing phenotypes. To date, no study has determined the mechanisms mediating this maternal effect's influence on offspring phenotype. However, levels of estrogen receptor alpha (ERα) gene expression are linked to differences in early growth and aggression; thus, maternal hormones may alter gene regulation, perhaps via DNA methylation, of ERα in offspring during prenatal development. We performed a pilot study to examine natural variation in testosterone allocation to offspring through egg yolks in wild Eastern Bluebirds (Sialia sialis) in varying breeding densities and percent DNA methylation of CG dinucleotides in the ERα promoter in offspring brain regions associated with growth and behavior. We hypothesized that breeding density would be positively correlated with yolk testosterone, and prenatal exposure to maternal‐derived yolk testosterone would be associated with greater offspring growth and decreased ERα promoter methylation. Yolk testosterone concentration was positively correlated with breeding density, nestling growth rate, and percent DNA methylation of one out of five investigated CpG sites (site 3) in the diencephalon ERα promoter, but none in the telencephalon (n = 10). Percent DNA methylation of diencephalon CpG site 3 was positively correlated with growth rate. These data suggest a possible role for epigenetics in mediating the effects of the maternal environment on offspring phenotype. Experimentally examining this mechanism with a larger sample size in future studies may help elucidate a prominent way in which animals respond to their environment. Further, by determining the mechanisms that mediate maternal effects, we can begin to understand the potential for the heritability of these mechanisms and the impact that maternal effects are capable of producing at an evolutionary scale.     

Evidence for inbreeding depression in a species with limited opportunity for maternal effects

It is often assumed that mating with close relatives reduces offspring fitness. In such cases, reduced offspring fitness may arise from inbreeding depression (i.e., genetic effects of elevated homozygosity) or from post‐mating maternal investment. This can be due to a reduction in female investment after mating with genetically incompatible males (“differential allocation”) or compensation for incompatibility (“reproductive compensation”). Here, we looked at the effects of mating with relatives on offspring fitness in mosquitofish, Gambusia holbrooki. In this species, females are assumed to be nonplacental and to allocate resources to eggs before fertilization, limiting differential allocation. We looked at the effects of mating with a brother or with an unrelated male on brood size, offspring size, gestation period, and early offspring growth. Mating with a relative reduced the number of offspring at birth, but there was no difference in the likelihood of breeding, gestation time, nor in the size or growth of these offspring. We suggest that due to limited potential for maternal effects to influence these traits that any reduction in offspring fitness, or lack thereof, can be explained by inbreeding depression rather than by maternal effects. We highlight the importance of considering the potential role of maternal effects when studying inbreeding depression and encourage further studies in other Poeciliid species with different degrees of placentation to test whether maternal effects mask or amplify any genetic effects of mating with relatives.     

Differential effects of offspring and maternal inbreeding on egg laying and offspring performance in the burying beetle Nicrophorus vespilloides

We investigate the effect of offspring and maternal inbreeding on maternal and offspring traits associated with early offspring fitness in the burying beetle Nicrophorus vespilloides. We conducted two experiments. In the first experiment, we manipulated maternal inbreeding only (keeping offspring outbred) by generating mothers that were outbred, moderately inbred or highly inbred. Meanwhile, in the second experiment, we manipulated offspring inbreeding only (keeping females outbred) by generating offspring that were outbred, moderately inbred or highly inbred. In both experiments, we monitored subsequent effects on breeding success (number of larvae), maternal traits (clutch size, delay until laying, laying skew, laying spread and egg size) and offspring traits (hatching success, larval survival, duration of larval development and average larval mass). Maternal inbreeding reduced breeding success, and this effect was mediated through lower hatching success and greater larval mortality. Furthermore, inbred mothers produced clutches where egg laying was less skewed towards the early part of laying than outbred females. This reduction in the skew in egg laying is beneficial for larval survival, suggesting that inbred females adjusted their laying patterns facultatively, thereby partially compensating for the detrimental effects of maternal inbreeding on offspring. Finally, we found evidence of a nonlinear effect of offspring inbreeding coefficient on number of larvae dispersing. Offspring inbreeding affected larval survival and larval development time but also unexpectedly affected maternal traits (clutch size and delay until laying), suggesting that females adjust clutch size and the delay until laying in response to being related to their mate.     

Body size-specific maternal effects on the offspring environment shape juvenile phenotypes in Atlantic salmon

Positive associations between maternal investment per offspring and maternal body size have been explained as adaptive responses by females to predictable, body size-specific maternal influences on the offspring’s environment. As a larger per-offspring investment increases maternal fitness when the quality of the offspring environment is low, optimal egg size may increase with maternal body size if larger mothers create relatively poor environments for their eggs or offspring. Here, we manipulate egg size and rearing environments (gravel size, nest depth) of Atlantic salmon (Salmo salar) in a 2 × 2 × 2 factorial experiment. We find that the incubation environment typical of large and small mothers can exert predictable effects on offspring phenotypes, but the nature of these effects provides little support to the prediction that smaller eggs are better suited to nest environments created by smaller females (and vice versa). Our data indicate that the magnitude and direction of phenotypic differences between small and large offspring vary among maternal nest environments, underscoring the point that removal of offspring from the environmental context in which they are provisioned in the wild can bias experimentally derived associations between offspring size and metrics of offspring fitness. The present study also contributes to a growing literature which suggests that the fitness consequences of egg size variation are often more pronounced during the early juvenile stage, as opposed to the egg or larval stage.     

Maternal effects on offspring size and number in mosquitofish,Gambusia holbrooki

Given a trade-off between offspring size and number, all mothers are predicted to produce the same optimal-sized offspring in a given environment. In many species, however, larger and/or older mothers produce bigger offspring. There are several hypotheses to explain this but they lack strong empirical support. In organisms with indeterminate growth, there is the additional problem that maternal size and age are positively correlated, so what are their relative roles in determining offspring size? To investigate this, we measured the natural relationship between maternal and offspring size in a wild population of Gambusia holbrooki (eastern mosquitofish), and experimentally disentangled the effects of maternal age and size on offspring size in the laboratory. In combination, our data indicate that the relationship between maternal and offspring size is nonlinear. Small mothers seem to produce larger than average offspring due to integer effects associated with very small broods. For extremely large mothers, which were only sampled in our wild data, these larger than average offspring may result from greater maternal resources or age effects. However, maternal age had no effect on offspring size or number in the laboratory experiment. Our results highlight the importance of sampling the full size–range of mothers when investigating maternal effects on offspring size. They also point to the difficulty of experimentally manipulating maternal size, because any change in size is invariably associated with a change in at least one factor affecting growth (be it temperature, food availability, or density) that might also have an indirect effect on offspring size.     

Exposure to exogenous egg cortisol does not rescue juvenile Chinook salmon body size,condition, or survival from the effects of elevated water temperatures

Climate change is leading to altered temperature regimes which are impacting aquatic life, particularly for ectothermic fish. The impacts of environmental stress can be translated across generations through maternally derived glucocorticoids, leading to altered offspring phenotypes. Although these maternal stress effects are often considered negative, recent studies suggest this maternal stress signal may prepare offspring for a similarly stressful environment (environmental match). We applied the environmental match hypothesis to examine whether a prenatal stress signal can dampen the effects of elevated water temperatures on body size, condition, and survival during early development in Chinook salmon Oncorhynchus tshawytscha from Lake Ontario, Canada. We exposed fertilized eggs to prenatal exogenous egg cortisol (1,000 ng/ml cortisol or 0 ng/ml control) and then reared these dosed groups at temperatures indicative of current (+0°C) and future (+3°C) temperature conditions. Offspring reared in elevated temperatures were smaller and had a lower survival at the hatchling developmental stage. Overall, we found that our exogenous cortisol dose did not dampen effects of elevated rearing temperatures (environmental match) on body size or early survival. Instead, our eyed stage survival indicates that our prenatal cortisol dose may be detrimental, as cortisol‐dosed offspring raised in elevated temperatures had lower survival than cortisol‐dosed and control reared in current temperatures. Our results suggest that a maternal stress signal may not be able to ameliorate the effects of thermal stress during early development. However, we highlight the importance of interpreting the fitness impacts of maternal stress within an environmentally relevant context.     

Giving offspring a head start in life: field and experimental evidence for selection on maternal basking behaviour in lizards

The timing of birth is often correlated with offspring fitness in animals, but experimental studies that disentangle direct effects of parturition date and indirect effects mediated via variation in female traits are rare. In viviparous ectotherms, parturition date is largely driven by female thermal conditions, particularly maternal basking strategies. Our field and laboratory studies of a viviparous lizard (Niveoscincus ocellatus) show that earlier‐born offspring are more likely to survive through their first winter and are larger following that winter, than are later‐born conspecifics. Thus, the association between parturition date and offspring fitness is causal, rather than reflecting an underlying correlation between parturition date and maternal attributes. Survival selection on offspring confers a significant advantage for increased maternal basking in this species, mediated through fitness advantages of earlier parturition. We discuss the roles of environmentally imposed constraints and parent–offspring conflict in the evolution of maternal effects on parturition date.     

Mothers influence offspring body size through post-oviposition maternal effects in the redbacked salamander, Plethodon cinereus

In the terrestrial salamander (Plethodon cinereus), previous work has shown that mothers body size is positively correlated to offspring size at the time of hatching even after controlling for the effects of egg size. This study was designed to determine whether maternal body size affects offspring size via pre-oviposition factors (e.g., yolk quality, jelly coat composition, or maternal genes) or post-oviposition factors (e.g., parental care behaviors, parental modification of environment). Gravid females were captured and induced to lay eggs in experimental chambers in which the environment was standardized. Fifteen clutches were exchanged, or cross-fostered, between female pairs differing in body size. Ten females whose eggs were taken away and then returned served as controls for the crossing treatment. Foster mothers did not significantly differ from control mothers in the time spent with eggs, body position, or number of egg movements during brooding. Average egg mass measured midway through development was not significantly correlated to the body size of either the genetic or foster mother, but was correlated to pre-oviposition oocyte size. At hatching, offspring body length was positively correlated to egg size and the foster mothers body size. This correlation suggests that in P. cinereus post-oviposition maternal effects have a greater impact on offspring size than other maternal factors incorporated into the egg prior to oviposition. While our study showed that larger mothers moved their eggs less often and tended to spend more time in contact with their eggs, further work needs to be done to identify the specific mechanisms through which larger mothers influence the body size of their offspring. This is the first experimental demonstration of post-oviposition maternal effects for any amphibian with parental care.     

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.     

Variable shrimp in variable environments: reproductive investment within Palaemon varians

The maternal environment may influence the quantity and quality of resources invested in offspring (per-offspring provisioning) and this trait, in turn, affects larval fitness and may carry-over into early juvenile life. Here, per-offspring investment was measured across three consecutive breeding seasons for the caridean shrimp, Palaemon varians. Egg and hatchling larval dry weight as well as hatchling larval biochemical composition were measured. Results indicate that egg volume is positively correlated with dry weight, but egg volume as a proxy for dry weight should be used with caution. Correlations were identified between per-offspring investment and average breeding season temperature, but the period over which temperature was averaged was important to whether these correlations were positive or negative, highlighting the complexity of identifying environmental influence on phenotypic traits. The most important factor determining offspring size and per-offspring investment was maternal size, which may be influenced by the environment as carapace length varied significantly between breeding seasons. These data demonstrate variation in egg and larval composition, related to maternal size, which will affect early life traits and survivorship for P. varians.

     

Premature birth stunts early growth and is a possible driver of stress-induced maternal effects in the guppy Poecilia reticulata

We tested the effects of gestational stress, principally in the form of alarm cue extracted from the skin of conspecifics, on reproduction in female guppies (Poecilia reticulata) and the growth and behaviour of their offspring. Offspring from mothers exposed to alarm cue exhibited stunted growth in the first few days post-partum, which appeared to be mediated by shortening of the gestation period, the length of which directly correlated with growth rate within the first 6 days post-partum. Mature offspring did not differ in behaviour or stress responses compared with controls and so the effects of maternal predation stress did not appear to persist into adulthood. A different form of gestational stress, dietary restriction, did not significantly affect offspring growth, though brood size was reduced, suggesting that the effects of predation stress were not mediated by differences in resource demand or consumption.     

Maternal effects are long‐lasting and influence female offspring's reproductive strategy in the swordtail fish Xiphophorus multilineatus

The adaptive benefits of maternal investment into individual offspring (inherited environmental effects) will be shaped by selection on mothers as well as their offspring, often across variable environments. We examined how a mother's nutritional environment interacted with her offspring's nutritional and social environment in Xiphophorus multilineatus, a live‐bearing fish. Fry from mothers reared on two different nutritional diets (HQ = high quality and LQ = low quality) were all reared on a LQ diet in addition to being split between two social treatments: exposed to a large adult male during development and not exposed. Mothers raised on a HQ diet produce offspring that were not only initially larger (at 14 days of age), but grew faster, and were larger at sexual maturity. Male offspring from mothers raised on both diets responded to the exposure to courter males by growing faster; however, the response of their sisters varied with mother's diet; females from HQ diet mothers reduced growth if exposed to a courter male, whereas females from LQ diet mothers increased growth. Therefore, we detected variation in maternal investment depending on female size and diet, and the effects of this variation on offspring were long‐lasting and sex specific. Our results support the maternal stress hypothesis, with selection on mothers to reduce investment in low‐quality environments. In addition, the interaction we detected between the mother's nutritional environment and the female offspring's social environment suggests that female offspring adopted different reproductive strategies depending on maternal investment.     

Quantitative genetics of costly neonatal sexual size dimorphism in squirrel monkeys (Saimiri boliviensis)

Offspring size is often an intimate link between the fitness of parents and offspring. Among mammals, neonate mass is also related to adult levels of dimorphism and intrasexual competitive mating. We describe the sex‐specific genetic architecture of neonate mass in captive squirrel monkeys (Saimiri boliviensis), a small Neotropical primate. Best fitting quantitative genetic models show strong maternal genetic effects with little difference between sexes offering limited opportunity for neonatal dimorphism to respond to observed or hypothetical selection. Heritabilities that are approximately zero also imply it is unlikely that neonatal dimorphism can evolve as a correlated response to selection on adult size. However, male mass is also more dependent on maternal condition (age and parity) making dimorphism plastic. Finally, we hypothesize that large maternal genetic effects reflect income breeding and tightly synchronized seasonal reproduction in squirrel monkeys, both of which require strong maternal control of offspring growth and timing of birth.     

Maternal investment in egg size: environment- and population-specific effects on offspring performance

Geographic variation in maternal investment in offspring size can be adaptive if differences in investment translate into improved offspring performance in the given environments. We compared two moor frog, Rana arvalis, populations in the laboratory to test the hypothesis that investment in large eggs in populations originating from stressful (acid) environments improves offspring performance when reared in stressful (acid) conditions. We found that large initial size (hatchling mass) had moderate to strong, environment-dependent positive effects on larval and metamorphic traits in the acidic origin population, but only weak effects in the neutral origin population. Our results suggest that interactions between environmental conditions and initial size can be important determinants of individual performance, and that investment in large eggs is adaptive in acid environments. These findings emphasize the role of maternal effects as adaptations to environmental stress.     

Sources of phenotypic variance in egg and larval traits in a marine invertebrate

Contrary to many separate sex systems, the evolutionary ecology of polyandry in simultaneous hermaphrodites, and in particular in those with internal fertilization, has received little attention. Recent studies on the promiscuous gastropod Chelidonura sandrana showed that offspring size, an important determinant of offspring performance in many marine invertebrates, varies with the number of different mating partners. However, the source of this differential allocation by mothers remained unclear. Using a quantitative genetic model, we here tested for parental effects on offspring size and the importance of ‘good gene’ effects on early life history traits. Our analysis revealed no significant sire but strong dam effects for all investigated traits. Moreover, embryo viability tended to increase with egg capsule volume, thus linking offspring size with offspring performance. Our findings suggest that in C. sandrana (1) differential allocation is a maternal effect in response to the number of different partners, and that (2) additive genetic variance is of negligible importance in early life history traits.     

Maternal influences on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination

Maternal and environmental factors are important sources of phenotypic variation because both factors influence offspring traits in ways that impact offspring and maternal fitness. The present study explored the effects of maternal factors (maternal body size, egg size, yolk‐steroid allocation, and oviposition‐site choice) and seasonally‐variable environmental factors on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination (Amphibolurus muricatus). Maternal identity had strong effects on offspring morphology, but the nature of maternal effects differed among successive clutches produced by females throughout the reproductive season (i.e. maternal identity by environment interactions). The among‐female and among‐clutch variation in offspring traits (including sex ratios) was not mediated through maternal body size, egg size, or variation in yolk steroid hormones. This lack of nongenetic maternal effects suggests that phenotypic variation may be generated by gene by environment interactions. These results demonstrate a significant genetic component to variation in offspring phenotypes, including sex ratios, even in species with environmental sex determination. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 256–266.     

Maternal Effects of Photoperiod and Food Level on Life History Characteristics of the Cladoceran Daphnia Pulicaria Forbes

The response of various life-history characteristics of Daphnia pulicaria to photoperiod and food concentration was measured in 16 combinations of maternal and offspring environments (long vs. short day, high vs. low food) in flow-through experiments. Response variables in offspring were time and survival to release of first offspring, clutch size and neonate mass in the first brood, mass of adult females after 30days and somatic growth rate during the course of the experiment. Most of these parameters were directly controlled by food concentration in the offspring environment, but maternal effects frequently modified the response. A long day length in the maternal environment resulted in a prolongation of the time to first clutch release in offspring similar to the direct effect of low food. Likewise, survival to maturation and female mass were affected by maternal photoperiod. Somatic growth rate and clutch size responded to combined effects of maternal food conditions and photoperiod. The laboratory results were used to predict the seasonal change of fecundity of Daphnia in the field. When data on clutch size are ordered in a sequence as the different combinations of maternal and offspring environment occur during the seasonal succession in a temperate lake, they show a bimodal distribution with a high peak in spring and a lower peak in fall. This pattern is consistent with field observations. We conclude that photoperiod and maternal effects are important factors influencing life history and population dynamics of Daphnia.     

Sex‐specific deposition and survival effects of maternal antibodies: a case study with the gull‐billed tern Gelochelidon nilotica

There is a growing body of evidence that maternal antibodies transferred to offspring have potential implications in the evolutionary ecology of birds. This transfer of maternal antibodies is a potentially flexible mechanism of non‐genetic inheritance by which mothers could favour some offspring over others and/or increase offspring survival, but this is a phenomenon that remains poorly understood. We examined sex‐specific deposition of maternal antibodies and its effects on early (5 d) and fledging (17 d) survival in semiprecocial chicks of the gull‐billed tern Gelochelidon nilotica, a long‐distance migratory bird. Mothers transferred a significantly greater amount of maternal antibodies to sons than to daughters. We found evidence for positive associations between maternal antibody levels at hatching and early offspring survival. This association might be sex‐specific, which can be understood as a mechanism of parental favouritism for the most sensitive sex.     

Variation in body size in the giant rhinoceros beetle Trypoxylus dichotomus is mediated by maternal effects on egg size

1. The egg size of insects can vary depending on maternal body size or resource status, and it may influence offspring body size by determining initial resource level. 2. The giant rhinoceros beetle Trypoxylus dichotomus exhibits considerable variation in body size, some of which is attributed to the variation in larval food (humus) quality, although a substantial amount of variation in body size remains unexplained. In the present study, changes in the egg size and offspring body size in response to several maternal variables were examined (i.e. body size, age, and, nutritional status). 3. Nutritional intake of the females during the adult stage did not affect the egg size. Larvae hatched from small eggs partially recovered from the initial disadvantage during their ontogenetic processes by increasing growth rate (i.e. compensatory growth); however, there was still a positive relationship between egg size and pupal body size. 4. Older females produced small eggs, but because of compensatory growth, the pupae were no longer small. By contrast, due to a lack of compensatory growth, small females produced small eggs as well as small pupae. 5. These results suggest that maternal body size affects offspring body size through effects on egg size. This transgenerational effect may account for some of the variation in adult body size of T. dichotomus.     

Direct and transgenerational effects of an experimental heatwave on early life stages in a freshwater snail

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