Postnatal Investment Research Articles

Mothers in a cooperatively breeding bird increase investment per offspring at the pre-natal stage when they will have more help with post-natal care.

In many cooperative societies, including our own, helpers assist with the post-natal care of breeders' young and may thereby benefit the post-natal development of offspring. Here, we present evidence of a novel mechanism by which such post-natal helping could also have beneficial effects on pre-natal development: By lightening post-natal maternal workloads, helpers may allow mothers to increase their pre-natal investment per offspring. We present the findings of a decade-long study of cooperatively breeding white-browed sparrow-weaver, Plocepasser mahali, societies. Within each social group, reproduction is monopolized by a dominant breeding pair, and non-breeding helpers assist with nestling feeding. Using a within-mother reaction norm approach to formally identify maternal plasticity, we demonstrate that when mothers have more female helpers, they decrease their own post-natal investment per offspring (feed their nestlings at lower rates) but increase their pre-natal investment per offspring (lay larger eggs, which yield heavier hatchlings). That these plastic maternal responses are predicted by female helper number, and not male helper number, implicates the availability of post-natal helping per se as the likely driver (rather than correlated effects of group size), because female helpers feed nestlings at substantially higher rates than males. We term this novel maternal strategy "maternal front-loading" and hypothesize that the expected availability of post-natal help either allows or incentivizes helped mothers to focus maternal investment on the pre-natal phase, to which helpers cannot contribute directly. The potential for post-natal helping to promote pre-natal development further complicates attempts to identify and quantify the fitness consequences of helping.

The social formation of fitness: lifetime consequences of prenatal nutrition and postnatal care in a wild mammal population.

Research in medicine and evolutionary biology suggests that the sequencing of parental investment has a crucial impact on offspring life history and health. Here, we take advantage of the synchronous birth system of wild banded mongooses to test experimentally the lifetime consequences to offspring of receiving extra investment prenatally versus postnatally. We provided extra food to half of the breeding females in each group during pregnancy, leaving the other half as matched controls. This manipulation resulted in two categories of experimental offspring in synchronously born litters: (i) 'prenatal boost' offspring whose mothers had been fed during pregnancy, and (ii) 'postnatal boost' offspring whose mothers were not fed during pregnancy but who received extra alloparental care in the postnatal period. Prenatal boost offspring lived substantially longer as adults, but postnatal boost offspring had higher lifetime reproductive success (LRS) and higher glucocorticoid levels across the lifespan. Both types of experimental offspring had higher LRS than offspring from unmanipulated litters. We found no difference between the two experimental categories of offspring in adult weight, age at first reproduction, oxidative stress or telomere lengths. These findings are rare experimental evidence that prenatal and postnatal investments have distinct effects in moulding individual life history and fitness in wild mammals. This article is part of the theme issue 'Evolutionary ecology of inequality'.

How does birth weight affect health and human capital? A short- and long-term evaluation.

In utero shocks have been shown to have long-lasting consequences. However, we hardly know whether these effects tend to fade out over time and whether they can be compensated by post-natal investments. This paper examines the effect of birth endowment over time by employing a long panel of individuals born in 1983 in Cebu (Philippines) that includes relevant information on the pregnancy. We build a refined health endowment measure netted out from prenatal investments. We find that initial endowments affect trajectories both through the human capital production function and subsequent parental investment. The effect of birth endowment remains until adulthood and the fading out is very limited for health outcomes but more pronounced for educational outcomes. We also find that parents tend to reinforce initial health endowments, but the effect of this behaviour has almost no effect on final outcomes.

The relationship between egg size and helper number in cooperative breeders: a meta-analysis across species.

BackgroundLife history theory predicts that mothers should adjust reproductive investment depending on benefits of current reproduction and costs of reduced future reproductive success. These costs and benefits may in turn depend on the breeding female’s social environment. Cooperative breeders provide an ideal system to test whether changes in maternal investment are associated with the social conditions mothers experience. As alloparental helpers assist in offspring care, larger groups might reduce reproductive costs for mothers or alternatively indicate attractive conditions for reproduction. Thus, mothers may show reduced (load-lightening) or increased (differential allocation) reproductive investment in relation to group size. A growing number of studies have investigated how cooperatively breeding mothers adjust pre-natal investment depending on group size. Our aim was to survey these studies to assess, first, whether mothers consistently reduce or increase pre-natal investment when in larger groups and, second, whether these changes relate to variation in post-natal investment.MethodsWe extracted data on the relationship between helper number and maternal pre-natal investment (egg size) from 12 studies on 10 species of cooperatively breeding vertebrates. We performed meta-analyses to calculate the overall estimated relationship between egg size and helper number, and to quantify variation among species. We also tested whether these relationships are stronger in species in which the addition of helpers is associated with significant changes in maternal and helper post-natal investment.ResultsAcross studies, there is a significant negative relationship between helper number and egg size, suggesting that in most instances mothers show reduced reproductive investment in larger groups, in particular in species in which mothers also show a significant reduction in post-natal investment. However, even in this limited sample, substantial variation exists in the relationship between helper number and egg size, and the overall effect appears to be driven by a few well-studied species.DiscussionOur results, albeit based on a small sample of studies and species, indicate that cooperatively breeding females tend to produce smaller eggs in larger groups. These findings on prenatal investment accord with previous studies showing similar load-lightening reductions in postnatal parental effort (leading to concealed helper effects), but do not provide empirical support for differential allocation. However, the considerable variation in effect size across studies suggests that maternal investment is mitigated by additional factors. Our findings indicate that variation in the social environment may influence life-history strategies and suggest that future studies investigating within-individual changes in maternal investment in cooperative breeders offer a fruitful avenue to study the role of adaptive plasticity.

The role of the mating system and intraspecific brood parasitism in the costs of reproduction in a passerine bird.

Limited resources trigger trade-offs in resource allocation. Reproduction is one of the most demanding activities in terms of energy, and costs related to reproduction can be apparent either as reduced future reproduction or as survival. However, costs are not always detected, because individual heterogeneity in quality and resource acquisition may explain variation in costs among individuals. We conducted a comprehensive study in spotless starlings (Sturnus unicolor) nesting in Central Spain to determine whether costs of reproduction could be detectable in the short and/or long term and whether prenatal or postnatal investment were driving these costs. We took into account the lifehistory of the species, where egg volume is highly repeatable, males are facultatively polygynous, and intraspecific brood parasitism occurs. Females with a high reproductive effort in a breeding event also had a high reproductive effort in the second event of the season. The mating system and maternal age were reliable predictors of breeding success within a breeding event: monogamous and primary females, as well as older mothers, raised more nestlings than secondary females and 1-year-old females, respectively. However, when high-investing females suffered intra-brood parasitism in 1 year, we found a negative correlation between current and futurereproduction. These results suggest that, under some circumstances, females are able to skip the short-term costs of reproduction, but when extra effort is added, trade-offs arise. While most studies have focused on different aspects of individual quality on costs, the ecological context seems to represent an important component that should be taken into account.

Birth order and health of newborns

We examine birth order differences in health of newborns and follow the children throughout childhood using high-quality administrative data on individuals born in Denmark between 1981 and 2010. Family fixed effects models show a positive and robust effect of birth order on health at birth; firstborn children are less healthy at birth. During earlier pregnancies, women are more likely to smoke, receive more prenatal care, and are more likely to suffer a medical pregnancy complication, suggesting worse maternal health. We further show that the health disadvantage of firstborns persists in the first years of life, disappears by age seven, and becomes a health advantage in adolescence. In contrast, later-born children are throughout childhood more likely to suffer an injury. The results on health in adolescence are consistent with previous evidence of a firstborn advantage in education and with the hypothesis that postnatal investments differ between first- and later-born children.

The Intergenerational Transmission of Low Birth Weight and Intrauterine Growth Restriction: A Large Cross-generational Cohort Study in Taiwan

Objectives Our research provides evidence on the intergenerational fetal programming effect by examining associations in the low birth weight (LBW, birth weight <2500g) and intrauterine growth restriction (IUGR) status between two adjacent generations from both the maternal and paternal sides. Methods Birth certificate data of the entire Taiwanese population are used to construct three-consecutive-generational samples. The final samples consist of the third-generation children born during 1999-2006 to at least one second-generation (G2) parent born during 1978-1985. Maternal and paternal samples are distinguished based on the gender of G2. We first fit the samples with linear probability models while including extensive explanatory variables to control for myriad confounding factors. We then include G2 sibling fixed effects to account for family-specific heterogeneity. Alternative explanations of sample selection, parents' assortative mating, and grandmothers' postnatal investment are examined. Results We find that significant intergenerational associations in LBW and IUGR only occur matrilineally. Children born to LBW mothers are 2.28 (95% CI, 0.71-3.85; p < 0.01) percentage points, corresponding to 36%, more likely to be LBW compared to children born to non-LBW mothers who are sisters. These associations cannot be explained by the above alternative explanations. Conclusions Under G2 sibling comparisons, children born to LBW (IUGR) mothers are more likely to be LBW (IUGR), but children born to LBW (IUGR) fathers are not. The findings suggest that maternal health is pertinent and that socio-economic interventions may not yield the desired outcomes within a short period of time.

Why do Mothers Harm their Babies? Evolutionary Perspectives

Young conspecifics are killed in many animal species, often by unrelated males. The role that females — particularly mothers — play in harming infants is often overlooked, as it appears an evolutionary paradox. Life-history theory offers potential explanations, as females are under pressure to time births optimally, produce an optimal number of offspring and secure paternal investment. Furthermore, socio-cultural circumstances across human societies may favour sex-specific infanticide. These constraints can lead mothers to terminate pre- or post-natal investment in current offspring. Incorporating evolutionary theory in policy making may offer opportunities to assess which measures are likely to reduce the rate of maternally committed infanticide.

Same Program, Different Outcomes: Understanding Differential Effects from Access to Free, High-Quality Early Care

The Infant Health and Development Program (IHDP) was designed to promote the development of low-birth weight (up to 2,500 grams) and premature (up to 37 weeks gestational age) infants. There is evidence that the IHDP intervention, a randomly-assigned bundle of services including primarily free, high-quality child care from 12 to 36 months, boosted cognitive and behavioral outcomes by the time participants at the end of the intervention. The literature has established that the intervention was more effective among the subsample of heavier low birth weight (2,000-2,500 grams) than among those born lighter. Among the heavier group, it was more effective for children from lower-income families. Families who participated in the intervention were diverse in key observable characteristics like income, race or ethnicity. In addition, families reallocated their time in different ways when then had the opportunity to use the free services provided by the IHDP. The goal of this paper is to understand the economic decisions and constraints faced by households who gained access to the IHDP and explain their differential behavior. In order to do so, we propose an economic model, construct measures of theoretically-relevant drivers of postnatal investment decisions, and explore patterns of heterogeneity in parental response and child development along these dimensions.

Sex ratio adjustment by sex-specific maternal cannibalism in hamsters

Mammalian offspring sex ratios can be biased via prenatal and postnatal mechanisms, including sperm selection, sex-specific embryo loss, and differential postnatal investment in males and females. Syrian hamsters routinely cannibalize some of their pups in the first days after birth. We present evidence that short day lengths, typically predictive of poor autumn and winter field conditions, are associated with male-biased sex ratios, achieved in part through selective perinatal maternal infanticide of female offspring. Higher peak litter sizes were associated with increased cannibalism rates, decreased final litter counts, and increased body mass of pups surviving to weaning. To our knowledge this is the first report of sex ratio adjustment by offspring cannibalism.

Explaining the Birth Order Effect: The Role of Prenatal and Early Childhood Investments

The critical role of prenatal and early childhood conditions on adult outcomes has been the focus of a rich body of research. In this paper, we examine various pre- and postnatal investments as possible sources behind the order effect – significant differences in the educational and labor market outcomes across children of varying birth orders. Taking advantage of a rich set of information on in utero and early childhood conditions in the Children of the NLSY79, we find that, within the same household, siblings of higher birth order experience a lower reduction in cigarette usage during pregnancy, are breastfed less often, and experience less cognitive stimulation and emotional support at ages 0 to 1. Next, we test for the presence of birth order effects in early cognitive and non-cognitive test scores and examine whether these differences can be explained by variations in prenatal and early childhood investments. Although there exists a significant negative relationship between birth order and early cognitive/non-cognitive test scores, the size and the significance of the negative birth order effects in test scores and educational attainment are robust to controlling for variations in early childhood factors.

Maternal condition does not influence birth sex ratios in anubis baboons (Papio anubis).

Trivers and Willard predicted that when parental condition has differential effects on the fitness of male and female offspring, parents who are in good condition will bias investment toward the sex that benefits most from additional investment. Efforts to test predictions derived from Trivers and Willard's model have had mixed results, perhaps because most studies have relied on proxy measures of parental condition, such as dominance rank. Here, we examine the effects of female baboons condition on birth sex ratios and post-natal investment, based on visual assessments of maternal body condition. We find that local environmental conditions have significant effects on female condition, but maternal condition at conception has no consistent relationship with birth sex ratios. Mothers who are in poorer condition at the time of conception resume cycling significantly later than females who are in better condition, but the sex of their infants has no effect on the time to resumption of cycling. Thus, our findings provide strong evidence that maternal condition influences females' ability to reproduce, but females do not facultatively adjust the sex ratio of their offspring in relation to their dominance rank or current condition.

Maternal investment and reproductive success in Chinese water deer

Abstract Among cervids, maternal investment, estimated as the amount of resources and care allocated to the offspring, was expected to be related to species body size. Therefore, maternal investment in a herd of captive Chinese water deer Hydropotes inermis, a relatively small species of cervid, was investigated over 3 years. Except during the lactation period, reproductive females spent about 2-fold more time resting than feeding. During lactation, the amount of time spent feeding increased highly (25.3 min/h during lactation vs 17.3 min/h during the gestation period). Females spent less than 30% of time in communal behaviours with offspring. They did not reject alien fawns during this care period. Frequency and duration of suckling events decreased exponentially from the second week onwards. More than 10% of suckling bouts were non-filial. Prenatal investment leads to a mean litter mass (about 12% of maternal mass) higher than in most cervid species. Postnatal investment in fawns represents a daily mass gain of ca. 85 g/d during the first 2 weeks, without any sexual difference. Female production, timing and synchrony of births and survival of fawns characterized reproductive success. Seventy percent of mature females gave birth, with a mean of 1.9 offspring per female. The sex ratio was even. Births were synchronous, 80% of births occurring in 25 days. In this herd, 0.74 fawn per female was successfully weaned and 0.56 fawn per female survived through their first year. Based on these results we conclude that reproductive strategy of Chinese water deer was efficient and characterized by mother-offspring relationships typical of hiders and high levels of pre- and postnatal investments. This strategy seems typical of small species of cervids without marked sexual dimorphism.

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.

An experimental examination of the consequences of communal versus solitary breeding on maternal condition and the early postnatal growth and survival of degu, Octodon degus, pups

Individuals of numerous rodent species engage in group living, in which they share an area of activity, a nest (or den), and interact more frequently with group members than with individuals from other such groups. Members of social groups may engage in communal breeding when they rear their young together in a common nest. We conducted an experimental study under laboratory conditions to explore the costs and benefits linked to early postnatal investment in offspring by female degus. In particular, we examined the quality and quantity of offspring produced by females rearing their litters in the presence of a second lactating (related or unrelated) female (‘communally breeding’) with offspring produced by lactating females in the presence of a nonbreeding (related or unrelated) female (‘singularly breeding’), and the offspring of solitary females. The physical condition of mothers (mass lost through lactation) was also examined. We studied 70 female degus and their litters, and 13 additional nonbreeding females, under constant conditions of adult density, nest availability, restricted food availability and breeding experience of subjects. The number of pups, the mass of pups, and the physical condition of mothers breeding communally did not differ from those of singularly and solitarily breeding females. Similar results were obtained when kinship of breeding females was considered. When reproductive performance of individuals within communally breeding groups was examined, we found that costs and benefits were not shared equally. Weanlings of litters born in the presence of a previous litter were smaller and less numerous than weanlings of litters born when no other young were present. Taken together, our results show that female degus derive no apparent reproductive benefits from early postnatal rearing of their offspring. Moreover, a proportion of females seem to pay a net cost.

Interannual variation in the post‐weaning and juvenile survival of subantarctic fur seals: influence of pup sex, growth rate and oceanographic conditions

SummaryA major hypothesis of life history theory is that early development conditions affect future survival and reproductive success. However, although a growing number of studies have addressed this question, many of them are taxonomically biased, thereby impeding the generalization of this hypothesis.This study examines the factors influencing post‐weaning survival in five weaned cohorts of subantarctic fur seal pups from Amsterdam Island, southern Indian Ocean. It used mark–recapture data from 7 consecutive years of different environmental conditions.The cohort return rate varied from 45% to 74% of weaned pups, depending on the year of weaning. In each cohort, 96% of weaned pups returned between 3 and 6 years of age, and none of the factors examined seemed to influence this timing pattern. The probability of survival to this first return was negatively related to sea‐surface temperature anomalies (SSTa) of the 6 months following the weaning process. It increased with pup preweaning growth rate and differed between the sexes. Females’ survival rate was significantly higher than males’, except during years of extreme SSTa, where no difference was detected.The juvenile state represented young individuals after their first return on their native island. Annual juvenile tag loss rate was constant at 0·217 (SE = 0·027), whereas temporary emigration rate varied over cohorts and was higher in males 0·423 (SE = 0·035) than in females 0·170 (SE = 0·012). This dispersion pattern may be prolonged in some cases, as the yearly immigration probability was constant at 0·290 (SE = 0·065).Taking into account tag loss and temporary emigration, the estimated yearly survival probability of juveniles was 0·964 (SE = 0·022). This value was unrelated to any tested oceanographic or individual parameter including sex.Results support the hypothesis that early development traits affect short‐term post‐weaning survival. However, no long‐term effect of maternal postnatal investment was detected after the first return to the native island. Results also indicate that the effect of early development traits on survival interacts with environmental conditions encountered shortly after independence of individuals.

Interpreting sex differences in enamel hypoplasia in human and non-human primates: Developmental, environmental, and cultural considerations.

The purpose of this review is to provide a synoptic, critical evaluation of the evidence of, and potential etiological factors contributing to, sex differences in the expression of enamel hypoplasia (EH). Specifically, this review considers theoretical expectations and empirical evidence bearing on two central issues. The first of these is the impact of a theorized inherent male vulnerability to physiological stress on sex differences in EH. The second issue is the potential contribution to sex differences in EH of intrinsic differences in male and female enamel composition and development. To address this first issue, EH frequencies by sex are examined in samples subject to a high degree of physiological stress. Based on the concept of inherent male vulnerability (or female buffering), males in stressful environments would be expected to exhibit higher EH frequencies than females. This expectation is evaluated in light of cultural practices of sex-biased investment that mediate the relationship between environmental stress and EH expression. Defects forming prenatally afford an opportunity to study this relationship without the confounding effects of sex-biased postnatal investment. Data bearing on this issue derive from previously conducted studies of EH in permanent and deciduous teeth in both modern and archaeological samples as well as from new data on Indian schoolchildren. To address the second issue, fundamental male-female enamel differences are evaluated for their potential impact on EH expression. A large sex difference in the duration of canine crown formation in non-human primates suggests that male canines may have greater opportunity to record stress events than those of females. This expectation is examined in great apes, whose canines often record multiple episodes of stress and are sexually dimorphic in crown formation times. With respect to the first issue, in most studies, sex differences in EH prevalence are statistically nonsignificant. However, when sex differences are significant, there is a slight trend for them to be greater in males than in females, suggesting a weak influence of greater male vulnerability. Cultural practices of sex-biased investment in children appear to have greater impact on EH expression than does male vulnerability/female buffering. With respect to the second issue, sex differences in the composition and development of enamel were reviewed and determined to have limited or unknown impact on EH expression. Of these factors, only the duration of crown formation was expected to affect EH expression by sex within the great apes. The data support an association between higher defect counts in the canines of great ape males relative to those of females that may be the result of longer crown formation times in the canines of great ape males. This review concludes with an assessment of the nature of the evidence currently available to examine these issues and suggests future avenues for research focused on elucidating them.

A COMPARATIVE INVESTIGATION OF HYAENID AND AARDWOLF LIFE-HISTORIES, WITH NOTES ON SPOTTED HYAENA MORTALITY PATTERNS

SUMMARY A comparative life-history analysis of the hyaenid genera (Crocuta, Hyaena and Proteles) reveals some unusual patterns for eutherian mammals. Developmental phases are not all positively related, suggesting a trade-off among variables. A gradient in lifestyles from early reproduction with few young per year (iteroparity) to late reproduction with many young per year (semelaparity) is apparent. In the genera Crocuta and Proteles an iteroparous lifestyle is associated with a relatively short gestation period and extensive postnatal investment in cubs, perhaps in response to potentially excessive juvenile mortality. Their major life-history features seem to form an adaptive complex serving to spread reproductive effort. These include: a reduced gestation period, precocial young and an early age at first reproduction. Furthermore, females of Crocuta sp. can conceive while lactating and display a relatively fast post-natal growth rate. These features collectively form a life-history strategy sharing muc...

Energetics, reproductive suppression and obligate communal breeding in carnivores

Social subordinates are reproductively suppressed in some communally breeding species, but not in others. Hypotheses for the evolution of reproductive suppression have focussed on ecological and demographic constraints limiting the benefits of attempting to breed as a subordinate. Factors determining the costs of breeding have received little attention. We use comparative data from communally breeding carnivores (Tables 1 to 5) to show that the energetic costs of reproduction may be a determinant of reproductive suppression. When costs are high, they are more likely to exceed the benefits of attempting reproduction as a subordinate, at which point subordinates should tolerate suppression. Specifically, we show that reproductive suppression is associated with costly gestation (P=0.027; Kruskal-Wallis test) and costly postnatal investment in litter growth (P=0.020; Kruskal-Wallis test).

Evidence of sex-biased postnatal maternal investment by Mongolian gerbils

Three experiments were undertaken examining the relative costs to female Mongolian gerbils, Meriones unguiculatus, of rearing four male or four female pups from birth to weaning. In experiment 1, it was observed that gerbil dams rearing all-male litters were almost twice as likely as gerbil dams rearing allfemale litters to be found: (1) with all their young in the nest throughout a 20-min observation period; and (2) with one or more pups attached to their nipples. In experiment 2, (1) dams rearing all-male litters delivered significantly fewer young as a consequence of impregnation during postpartum oestrus than did dams rearing all-female litters and (2) dams rearing all-male litters exhibited both significantly greater periods of vaginal closure (preventing copulation) and significantly greater inter-litter intervals than did dams rearing all-female litters. In experiment 3, it was found that vaginal closure also provides an index of whether a gerbil dam will transfer milk to her pups. Consequently, the greater durations of vaginal closure observed in dams rearing all-male litters than in dams rearing all-female litters (experiment 2) suggest a longer period of milk transfer from dams to their male than to their female young before weaning. The data were interpreted as consistent with the hypothesis that rearing male pups was more costly to gerbil dams than was rearing female pups. Difficulties in determining the relative cost to dams of rearing male and female young were discussed.