Dynamic influence of maternal and pup traits on maternal care during lactation in an income breeder, the antarctic fur seal

Life-history theory predicts that selection will favor optimal levels of parental effort that balance benefits of current reproduction with costs to survival and future reproduction. The optimal level of effort depends on parental traits, offspring traits, and provisioning strategy. Additionally, how these factors influence effort may differ depending on the stage of reproduction. The relative importance of maternal and offspring traits on energy allocation to offspring was investigated in known-age Antarctic fur seals Arctocephalus gazella across four stages of reproduction, using birth mass and milk-consumption measurements. Maternal traits were important during three of the four stages investigated, with larger females giving birth to larger pups and investing more in pups during perinatal and molt stages. Pup mass influenced maternal effort during the premolt stage, and provisioning strategy influenced postnatal maternal effort at all stages. Energy provided to the offspring during an attendance visit was positively related to the duration of the foraging-trip/visit cycle; however, when investment was controlled for trip/visit cycle duration, the overall rate of energy transfer was similar across trip durations. In addition to strong effects of maternal mass, pup traits affected energy allocation, suggesting that pup demand is important in determining maternal care. These findings emphasize the importance of considering state variables in life-history studies and suggest that timing of measurements of effort in species with long provisioning periods may influence conclusions and our ability to make comparisons of reproductive effort among species.     

Are species differences in maternal effects arising from maternal care adaptive?

Parental care benefits offspring through maternal effects influencing their development, growth and survival. However, although parental care in general is likely the result of adaptive evolution, it does not follow that specific differences in the maternal effects that arise from care are also adaptive. Here, we used an interspecific cross‐fostering design in the burying beetle species Nicrophorus orbicollis and N. vespilloides, both of which have elaborate parental care involving direct feeding of regurgitated food to offspring, to test whether maternal effects are optimized within a species and therefore adaptive. Using a full‐factorial design, we first demonstrated that N. orbicollis care for offspring longer regardless of recipient species. We then examined offspring development and mass in offspring reared by hetero‐ or conspecific parents. As expected, there were species‐specific direct effects independent of the maternal effects, as N. orbicollis larvae were larger and took longer to develop than N. vespilloides regardless of caregiver. We also found significant differences in maternal effects: N. vespilloides maternal care caused more rapid development of offspring of either species. Contrary to expectations if maternal effects were species‐specific, there were no significant interactions between caretaker and recipient species for either development time or mass, suggesting that these maternal effects are general rather than optimized within species. We suggest that rather than coadaptation between parents and offspring performance, the species differences in maternal effects may be correlated with direct effects, and that their evolution is driven by selection on those direct effects.     

Maternal care,mother–offspring aggregation and age‐dependent coadaptation in the European earwig

Benefits and costs of parental care are expected to change with offspring development and lead to age‐dependent coadaptation expressed as phenotypic (behavioural) matches between offspring age and parental reproductive stage. Parents and offspring interact repeatedly over time for the provision of parental care. Their behaviours should be accordingly adjusted to each other dynamically and adaptively, and the phenotypic match between offspring age and parental stage should stabilize the repeated behavioural interactions. In the European earwig (Forficula auricularia), maternal care is beneficial for offspring survival, but not vital, allowing us to investigate the extent to which the stability of mother–offspring aggregation is shaped by age‐dependent coadaptation. In this study, we experimentally cross‐fostered nymphs of different age classes (younger or older) between females in early or late reproductive stage to disrupt age‐dependent coadaptation, thereby generating female–nymph dyads that were phenotypically matched or mismatched. The results revealed a higher stability in aggregation during the first larval instar when care is most intense, a steeper decline in aggregation tendency over developmental time and a reduced developmental rate in matched compared with mismatched families. Furthermore, nymph survival was positively correlated with female–nymph aggregation stability during the early stages when maternal care is most prevalent. These results support the hypothesis that age‐related phenotypically plastic coadaptation affects family dynamics and offspring developmental rate.     

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.     

Age-related body weight constraints on prenatal and milk provisioning in Iberian red deer (Cervus elaphus hispanicus) affect allocation of maternal resources

Maternal phenotypic characteristics can influence key life history variables of their offspring through maternal effects. In this study, we examined how body size constraints on maternal weight in yearling and subadult compared to adult hinds (age class effects) affected prenatal (calf birth weight, calf to hind weight ratio) and postnatal (milk) provisioning of Iberian red deer calves. Age correlated with all prenatal and postnatal investment traits except calf gains, although correlations were weaker than those with maternal weight. Once the effect of linear increase in weight with age was removed from models, yearlings showed additional reductions in calf birth weight, calf gains, and milk provisioning. The low-calf birth weight might increase the risk of calf mortality during lactation, as this occurs primarily during the first day of life and is strongly related to birth weight. Yearlings showed a greater prenatal allocation of resources in terms of greater calf to hind weight ratio probably as an extra effort by yearling mothers to balance calf neonatal mortality. It might compensate young mothers to produce low-quality calves while still growing rather than waiting for the uncertain possibility of surviving to the next reproductive season.     

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.     

Factors affecting weaning weight in Antarctic fur seals Arctocephalus gazella at South Georgia

Summary Relationships between size, body condition, age and feeding-attendance patterns during pup rearing of female Antacrtic fur seals Arctocephalus gazella and their effects on the timing of birth and weaning, pup weight, growth and condition were studied at South Georgia in 1981–1982. Twenty-seven (6 male, 21 female) mother-pup pairs were followed from birth to weaning. The analysis of maternal effects was limited to female pups because of the small sample size of male weaners. High weaning weight was associated with those female pups whose mothers spent more time ashore attending their offspring. Weaning weight showed no relationship with perinatal duration, number of feeding trips to sea, days at sea or date of weaning. A further 63 mother-pup pairs were analysed for the effects of maternal body condition (weight/length), age and timing of birth on offspring body weight and condition. Pup weight and condition were weakly correlated with maternal age in female pups. Male pups born earlier in the season were heavier and in better condition. Maternal and offspring body weight and condition were unrelated. For the Antarctic fur seal population at South Georgia where the food supply was apparently not limiting in summer, maternal condition and foraging time were subordinate to maternal care on land (as expressed by attendance duration) in determining offspring weight at weaning.     

Direct and indirect effects of environmental temperature on the evolution of reproductive strategies: an information-theoretic approach

For ectotherms, environmental temperature affects the optimal size and number of offspring via multiple mechanisms. First, temperature influences the performance of offspring, which directly affects the optimal size of offspring. Second, temperature influences maternal body size, which indirectly affects the optimal size and/or number of offspring when larger females acquire more energetic resources or provide better parental care. Although traditional statistical approaches might distinguish the relative importance of these effects, an information-theoretic approach enables one to estimate effects more accurately by identifying the best evolutionary model in a set of candidate models. Here, we use the Akaike Information Criterion to calculate the likelihoods of seven path models, each derived from one or more optimality models of reproduction. Variation in reproductive traits among populations of lizards (Sceloporus undulatus) was used to quantify support for the models. Our results overwhelmingly supported a model based on an indirect effect of temperature that is mediated by maternal size. Path coefficients of this model were consistent with the hypotheses that, first, larger females can acquire more energy for reproduction and, second, the survival of offspring depends on both their size and their density. Our analyses exemplify how information theory can identify evolutionary hypotheses that merit experimental testing.     

Offspring size and timing of hatching determine survival and reproductive output in a lizard

Selection on offspring size and timing of birth or hatching could have important consequences for maternal investment strategies. Here we show consistent viability selection on hatchling body length across 2 consecutive years in a lizard that lays several clutches per season. There was no effect of hatching date on survival to maturity. However, both early hatching and large hatchling size increased adult size, which has a positive effect on total reproductive output. Earlier hatching also led to an earlier onset of reproduction. Overall, increased survival probability for large hatchlings and a positive effect of clutch size on recruitment suggest consistent directional selection on both egg size and clutch size within and across years. Because offspring size and timing of hatching are strongly affected by environmental and maternal effects, there should be potential for strong transgenerational effects on reproductive output in this species. We briefly discuss the implications of these results for the evolutionary ecology of maternal investment and population fluctuations in short-lived lizards.     

Age affects the expression of maternal care and subsequent behavioural development of offspring in a precocial bird

Variations of breeding success with age have been studied largely in iteroparous species and particularly in birds: survival of offspring increases with parental age until senescence. Nevertheless, these results are from observations of free-living individuals and therefore, it remains impossible to determine whether these variations result from parental investment or efficiency or both, and whether these variations occur during the prenatal or the postnatal stage or during both. Our study aimed first, to determine whether age had an impact on the expression of maternal breeding care by comparing inexperienced female birds of two different ages, and second, to define how these potential differences impact chicks' growth and behavioural development. We made 22 2-month-old and 22 8-month-old female Japanese quail foster 1-day-old chicks. We observed their maternal behaviour until the chicks were 11 days old and then tested these chicks after separation from their mothers. Several behavioural tests estimated their fearfulness and their sociality. We observed first that a longer induction was required for young females to express maternal behaviour. Subsequently as many young females as elder females expressed maternal behaviour, but young females warmed chicks less, expressed less covering postures and rejected their chicks more. Chicks brooded by elder females presented higher growth rates and more fearfulness and sociality. Our results reveal that maternal investment increased with age independently of maternal experience, suggesting modification of hormone levels implied in maternal behaviour. Isolated effects of maternal experience should now be assessed in females of the same age. In addition, our results show, for first time in birds, that variations in maternal care directly induce important differences in the behavioural development of chicks. Finally, our results confirm that Japanese quail remains a great laboratory model of avian maternal behaviour and that the way we sample maternal behaviour is highly productive.     

Relations among birth condition, maternal condition, and postnatal growth in captive common marmoset monkeys (Callithrix jacchus)

The present study characterizes the relations among maternal condition, litter size, birth condition, and growth in body weight for a population of common marmosets. The subjects of the study were marmosets born into a single colony between 1994 and 2001. Three sets of analyses were conducted to answer the following questions: 1) Is there a relationship between litter size, maternal condition, and birth condition? In the study population, maternal body weight, maternal age, litter size, and birth condition were related in a complex fashion. Birth weight and prenatal long‐bone growth, as reflected in knee–heel length, were both related to maternal age, with older mothers supporting higher prenatal growth. Age and maternal condition appeared to interact as determinants of long‐bone growth, as the combination of older and larger mothers resulted in significantly longer knee–heel lengths in their offspring. 2) Is there a relationship between birth condition or maternal condition and subsequent growth or final adult size? The early growth rate in this population was similar to early growth rates reported for three different marmoset colonies, suggesting that early growth may be relatively inflexible in this species. However, within this population, the variation that did occur in early growth rate was related to birth weight and maternal weight. Later growth and adult weight were related to birth weight and litter size: small twin infants displayed slower later growth rates and were smaller as adults than twins that began life at a higher birth weight, while the birth weight of triplets was not related to adult size. In these marmosets, small infants that were the result of increased litter size differed from small infants whose small birth size resulted from other factors. This reinforces the proposal that the causes of low birth weight will be relevant to the development of the marmoset as a model of prenatal environmental effects. Am. J. Primatol. 62:83–94, 2004. © 2004 Wiley‐Liss, Inc.     

Parasite resistance and parasite tolerance: insights into transgenerational immune priming in an invertebrate host

Parasites impose different selection regimes on their hosts, which respond by increasing their resistance and/or tolerance. Parental challenge with parasites can enhance the immune response of their offspring, a phenomenon documented in invertebrates and termed transgenerational immune priming. We exposed two parental generations of the model organism Daphnia magna to the horizontally transmitted parasitic yeast Metschnikowia bicuspidata and recorded resistance- and tolerance-related traits in the offspring generation. We hypothesized that parentally primed offspring will increase either their resistance or their tolerance to the parasite. Our susceptibility assays revealed no impact of parental exposure on offspring resistance. Nonetheless, different fitness-related traits, which are indicative of tolerance, were altered. Specifically, maternal priming increased offspring production and decreased survival. Grandmaternal priming positively affected age at first reproduction and negatively affected brood size at first reproduction. Interestingly, both maternal and grandmaternal priming significantly reduced within-host–parasite proliferation. Nevertheless, Daphnia primed for two consecutive generations had no competitive advantage in comparison to unprimed ones, implying additive maternal and grandmaternal effects. Our findings do not support evidence of transgenerational immune priming from bacterial infections in the same host species, thus, emphasizing that transgenerational immune responses may not be consistent even within the same host species.     

When it is costly to have a caring mother: food limitation erases the benefits of parental care in earwigs

The aggregation of parents with offspring is generally associated with different forms of care that improve offspring survival at potential costs to parents. Under poor environments, the limited amount of resources available can increase the level of competition among family members and consequently lead to adaptive changes in parental investment. However, it remains unclear as to what extent such changes modify offspring fitness, particularly when offspring can survive without parents such as in the European earwig, Forficula auricularia. Here, we show that under food restriction, earwig maternal presence decreased offspring survival until adulthood by 43 per cent. This effect was independent of sibling competition and was expressed after separation from the female, indicating lasting detrimental effects. The reduced benefits of maternal presence on offspring survival were not associated with higher investment in future reproduction, suggesting a condition-dependent effect of food restriction on mothers and local mother-offspring competition for food. Overall, these findings demonstrate for the first time a long-term negative effect of maternal presence on offspring survival in a species with maternal care, and highlight the importance of food availability in the early evolution of family life.     

Offspring of older parents are smaller—but no less bilaterally symmetrical—than offspring of younger parents in the aquatic plant Lemna turionifera

Offspring quality decreases with parental age in many taxa, with offspring of older parents exhibiting reduced life span, reproductive capacity, and fitness, compared to offspring of younger parents. These “parental age effects,” whose consequences arise in the next generation, can be considered as manifestations of parental senescence, in addition to the more familiar age‐related declines in parent‐generation survival and reproduction. Parental age effects are important because they may have feedback effects on the evolution of demographic trajectories and longevity. In addition to altering the timing of offspring life‐history milestones, parental age effects can also have a negative impact on offspring size, with offspring of older parents being smaller than offspring of younger parents. Here, we consider the effects of advancing parental age on a different aspect of offspring morphology, body symmetry. In this study, we followed all 403 offspring of 30 parents of a bilaterally symmetrical, clonally reproducing aquatic plant species, Lemna turionifera, to test the hypothesis that successive offspring become less symmetrical as their parent ages, using the “Continuous Symmetry Measure” as an index. Although successive offspring of aging parents older than one week became smaller and smaller, we found scant evidence for any reduction in bilateral symmetry.     

Parental antagonism and parent-offspring co-adaptation interact to shape family life

The family is an arena for conflicts between offspring, mothers and fathers that need resolving to promote the evolution of parental care and the maintenance of family life. Co-adaptation is known to contribute to the resolution of parent-offspring conflict over parental care by selecting for combinations of offspring demand and parental supply that match to maximize the fitness of family members. However, multiple paternity and differences in the level of care provided by mothers and fathers can generate antagonistic selection on offspring demand (mediated, for example, by genomic imprinting) and possibly hamper co-adaptation. While parent-offspring co-adaptation and parental antagonism are commonly considered two major processes in the evolution of family life, their co-occurrence and the evolutionary consequences of their joint action are poorly understood. Here, we demonstrate the simultaneous and entangled effects of these two processes on outcomes of family interactions, using a series of breeding experiments in the European earwig, Forficula auricularia, an insect species with uniparental female care. As predicted from parental antagonism, we show that paternally inherited effects expressed in offspring influence both maternal care and maternal investment in future reproduction. However, and as expected from the entangled effects of parental antagonism and co-adaptation, these effects critically depended on postnatal interactions with caring females and maternally inherited effects expressed in offspring. Our results demonstrate that parent-offspring co-adaptation and parental antagonism are entangled key drivers in the evolution of family life that cannot be fully understood in isolation.     

Sedentary behavior during postnatal life is determined by the prenatal environment and exacerbated by postnatal hypercaloric nutrition

The discovery of a link between in utero experience and later metabolic and cardiovascular disease is one of the most important advances in epidemiology research of recent years. There is now increasing evidence that alterations in the fetal environment have long-term consequences on metabolic and endocrine pathophysiology in adult life. This process has been termed "fetal programming," and we have shown that undernutrition of the mother during gestation leads to obesity, hypertension, hyperphagia, hyperinsulinemia, and hyperleptinemia in offspring. Using this model of maternal undernutrition throughout pregnancy, we investigated whether prenatal influences may lead to alterations in postnatal locomotor behavior, independent of postnatal nutrition. Virgin Wistar rats were time mated and randomly assigned to receive food either ad libitum (ad libitum group) or at 30% of ad libitum intake (undernourished group). Offspring from UN mothers were significantly smaller at birth than AD offspring. At weaning, offspring were assigned to one of two diets [control or hypercaloric (30% fat)]. At ages of 35 days, 145 days, and 420 days, voluntary locomotor activity was assessed. At all ages studied, offspring from undernourished mothers were significantly less active than offspring born of normal birth weight for all parameters measured, independent of postnatal nutrition. Sedentary behavior in programmed offspring was exacerbated by postnatal hypercaloric nutrition. This work is the first to clearly separate prenatal from postnatal effects and shows that lifestyle choices themselves may have a prenatal origin. We have shown that predispositions to obesity, altered eating behavior, and sedentary activity are linked and occur independently of postnatal hypercaloric nutrition. Moreover, the prenatal influence may be permanent as offspring of undernourished mothers were still significantly less active compared with normal offspring at an advanced adult age, even in the presence of a healthy diet throughout postnatal life.     

Maternal investment during pregnancy in wild meerkats

Maternal investment in offspring development is a major determinant of the survival and future reproductive success of both the mother and her young. Mothers might therefore be expected to adjust their investment according to ecological conditions in order to maximise their lifetime fitness. In cooperatively breeding species, where helpers assist breeders with offspring care, the size of the group may also influence maternal investment strategies because the costs of reproduction are shared between breeders and helpers. Here, we use longitudinal records of body mass and life history traits from a wild population of meerkats (Suricata suricatta) to explore the pattern of growth in pregnant females and investigate how the rate of growth varies with characteristics of the litter, environmental conditions, maternal traits and group size. Gestational growth was slight during the first half of pregnancy but was marked and linear from the midpoint of gestation until birth. The rate of gestational growth in the second half of pregnancy increased with litter size, maternal age and body mass, and was higher for litters conceived during the peak of the breeding season when it is hot and wet. Gestational growth rate was lower in larger groups, especially when litter size was small. These results suggest that there are ecological and physiological constraints on gestational growth in meerkats, and that females may also be able to strategically adjust their prenatal investment in offspring according to the likely fitness costs and benefits of a particular breeding attempt. Mothers in larger groups may benefit from reducing their investment because having more helpers might allow them to lower reproductive costs without decreasing breeding success.     

A model for optimal offspring size in fish, including live-bearing and parental effects

Since Smith and Fretwell's seminal article in 1974 on the optimal offspring size, most theory has assumed a trade-off between offspring number and offspring fitness, where larger offspring have better survival or fitness, but with diminishing returns. In this article, we use two ubiquitous biological mechanisms to derive the shape of this trade-off: the offspring's growth rate combined with its size-dependent mortality (predation). For a large parameter region, we obtain the same sigmoid relationship between offspring size and offspring survival as Smith and Fretwell, but we also identify parameter regions where the optimal offspring size is as small or as large as possible. With increasing growth rate, the optimal offspring size is smaller. We then integrate our model with strategies of parental care. Egg guarding that reduces egg mortality favors smaller or larger offspring, depending on how mortality scales with size. For live-bearers, the survival of offspring to birth is a function of maternal survival; if the mother's survival increases with her size, then the model predicts that larger mothers should produce larger offspring. When using parameters for Trinidadian guppies Poecilia reticulata, differences in both growth and size-dependent predation are required to predict observed differences in offspring size between wild populations from high- and low-predation environments.     

Costs of reproduction and terminal investment by females in a semelparous marsupial

Evolutionary explanations for life history diversity are based on the idea of costs of reproduction, particularly on the concept of a trade-off between age-specific reproduction and parental survival, and between expenditure on current and future offspring. Such trade-offs are often difficult to detect in population studies of wild mammals. Terminal investment theory predicts that reproductive effort by older parents should increase, because individual offspring become more valuable to parents as the conflict between current versus potential future offspring declines with age. In order to demonstrate this phenomenon in females, there must be an increase in maternal expenditure on offspring with age, imposing a fitness cost on the mother. Clear evidence of both the expenditure and fitness cost components has rarely been found. In this study, we quantify costs of reproduction throughout the lifespan of female antechinuses. Antechinuses are nocturnal, insectivorous, forest-dwelling small (20-40 g) marsupials, which nest in tree hollows. They have a single synchronized mating season of around three weeks, which occurs on predictable dates each year in a population. Females produce only one litter per year. Unlike almost all other mammals, all males, and in the smaller species, most females are semelparous. We show that increased allocation to current reproduction reduces maternal survival, and that offspring growth and survival in the first breeding season is traded-off with performance of the second litter in iteroparous females. In iteroparous females, increased allocation to second litters is associated with severe weight loss in late lactation and post-lactation death of mothers, but increased offspring growth in late lactation and survival to weaning. These findings are consistent with terminal investment. Iteroparity did not increase lifetime reproductive success, indicating that terminal investment in the first breeding season at the expense of maternal survival (i.e. semelparity) is likely to be advantageous for females.