Effects of early experience on female behavioural and reproductive development in rhesus macaques

A growing body of research on humans suggests that exposure to a stressful family environment or father absence from home during childhood is associated with early female puberty and greater interest in infants among adolescent girls. This effect may be mediated by early exposure to harsh and inconsistent maternal care, but the mechanisms by which maternal care affects female reproductive maturation are not known. The present study reports sex differences in interest in infants among juvenile rhesus macaques similar to those observed in human adolescents. Furthermore, juvenile females that were exposed to harsh and inconsistent maternal care in infancy showed higher interest in infants than controls. Evidence from cross-fostered females indicated that these effects resulted from early experience and not genetic inheritance from the mother. There were no significant differences in female age at first conception in relation to the quality of maternal care received during infancy. Macaque females exposed to harsh and inconsistent maternal care in infancy tended to have higher cortisol responses to stress and to corticotropin-releasing hormone than controls in the first three years of life. Furthermore, females with higher cortisol responses to stress exhibited higher interest in infants. These findings suggest that some of the effects of early parental care on female reproductive maturation may be mediated by developmental changes in the activity of the hypothalamic-pituitary-adrenal axis.     

Natal Attraction in Adult Female Baboons (Papio cynocephalus ursinus) in the Moremi Reserve, Botswana

Mammalian females are strongly attracted to infants and interact regularly with them. Female baboons make persistent attempts to touch, nuzzle, smell and inspect other females’ infants, but do not hold them for long periods, carry them, or provide other kinds of care for them. Mothers generally tolerate these interactions, but never initiate them. The function of these brief alloparental interactions is not well understood. Infant handling might be a form of reproductive competition if females’ interest in infants causes distress to mothers or harm to their infants. Alternatively, infant handling might be the product of selection for appropriate maternal care if females who are highly responsive to infants are the most successful mothers. We test several predictions derived from these hypotheses with data collected in a free‐ranging group of baboons (Papio cynocephalus ursinus) in the Moremi Reserve of Botswana. Infants were most attractive when they were very young. Mothers of young infants were approached by other adult females on average once every 6 min, and other females attempted to handle their infants approximately once every 9 min. By the time infants were a year old, their mothers were being approached only once every 30 min and infants were being handled only once every 5 h. Females were more strongly attracted to other females’ infants when they had young infants of their own, and their interest in other females’ infants declined as their own infants matured. Females seemed to be equally attracted to all infants, but had greater access to offspring of their relatives and subordinate females. Females nearly always grunted as they handled infants. As in other contexts grunts are a reliable predictive signal that non‐aggressive behavior will follow, the use of grunts before handling suggests that these interactions were not a form of deliberate harassment.     

Reproduction in wild female olive baboons

The purpose of this paper is to evaluate several factors that influence female reproduction in a large troop of wild olive baboons (Papio cynocephalus anubis) based on 4 consecutive years of demographic data. Interbirth intervals were significantly shorter for females whose infants died before their next conception than for females whose infants survived. High-ranking mothers of surviving infants had significantly shorter birth intervals than comparable low-ranking mothers, independent of maternal age. This occurred mainly because the interval from resumption of cycling to conception was significantly shorter for high-vs. low-ranking females. Dominance rank did not influence sex ratio at birth, infant survival in the first 2 years, or adult female mortality. Age was also significantly related to interbirth intervals, with older females having shorter intervals. Primiparous females had consistently longer reproductive intervals than did multiparous females, but this difference reached statistical significance only for females whose infants died before the next conception. Primiparous females also experienced significantly higher infant mortality. Data on body size and estrous cycle length indicated no differences between high- and low-ranking females. Nutritional and stress-related mechanisms that may underlie the reproductive advantages of high rank are discussed.     

Growth in colony living anubis baboon infants and its relationship with maternal activity budgets and reproductive status

Early growth is of interest because it is susceptible to maternal effects and linked to fitness components for a range of species. Here we present anthropometric measurements on 23 infant olive baboons born into a captive colony in order to describe growth over the first 2 years of life, to explore maternal influences on growth, and to assess the impact of growth profiles on maternal reproduction. Six main findings emerged: 1) Infant growth rates in our colony were higher than those reported for wild populations but comparable to those observed for food-enhanced animals. 2) The ratio of infant mass to maternal mass was positively associated with reproductive parameters, such as duration of post-partum amenorrhea and interbirth interval. 3) Mothers resumed cycling and reconceived when their infants attained a relatively consistent threshold mass. 4) Infant mass-for-age was associated with maternal rank and, independently, with maternal mass such that females of high dominance rank and heavy females had relatively large infants at their resumption of cycling. 5) Low-ranking and lighter females had longer investment periods but smaller infants. They continued investment in infant through prolonged lactation until their infants reached a mass similar to that of infants of high-ranking/heavy mothers, suggesting that the lengthening of investment is essentially compensatory for slow early growth. 6) There was no relationship between infant growth and maternal activity budgets. Maternal physical and social factors, not energetics, contributed to differences among infants in growth trajectories, and infant growth temporally influenced successive reproductive events.     

Further hormonal suppression of eldest daughter cotton-top tamarins following birth of infants

Reproductive suppression of females is found throughout the Callitrichids. However, in many species some evidence of ovarian activity is observed in subordinate females. Subordinate cotton-top tamarin females in our colony have never been observed to ovulate in the presence of a reproductive female. However, ovarian follicular development does occur, and measurable levels of urinary estrogen and luteinizing hormone are frequently found in subordinate females. We studied 11 female tamarins living in family groups with a reproductive female. Each of the 8 eldest daughters had measurable urinary estrogen and LH levels and showed a reduction of hormonal levels when new infants were born. The 3 younger daughters showed barely detectable hormonal levels that did not change. Following the birth of infants the eldest daughters scent marked less frequently, increased time in contact with and grooming group members other than the mother, but they were more often targets of aggression than immediately prior to infant births. The eldest daughters were somewhat less involved in care of new infants than expected, although they spent much time in proximity to those carrying the infants. These results suggest that the further reduction of hormonal levels in subordinate females after the birth of infants may function to prevent these females from competing with mothers during the post-partum estrus rather than recruiting the eldest daughters as helpers for infant care. © 1993 Wiley-Liss, Inc.     

Diminished maternal responsiveness during pregnancy in multiparous female common marmosets

Common marmoset monkeys (Callithrix jacchus) live in small groups in which, usually, only a single female breeds and all group members provide infant care. When two females breed concurrently, however, they may commonly kill one another's infants, especially during the peripartum period. To investigate the mechanisms underlying infanticide by breeding females, we characterized responses of multiparous females to infants and determined circulating hormone levels in adult females during early pregnancy, late pregnancy, and the early postpartum period. Additionally, we compared the responses of postpartum females to their own infants and infants of other females (unfamiliar infants). Postpartum females were highly maternal toward both their own and unfamiliar infants, and showed no differences in their behavioral or hormonal responses to the two. During both early and late pregnancy, however, these females exhibited longer latencies to initially approach unfamiliar infants and spent less time carrying unfamiliar infants. Moreover, females spent less time carrying unfamiliar infants during late pregnancy than early pregnancy. Most late pregnant females never carried infants, and those that did rejected them quickly. Prolactin concentrations were higher and progesterone concentrations lower postpartum than in early or late pregnancy, while estradiol concentrations, the estradiol-to-progesterone ratio, and cortisol levels were higher during late pregnancy. Within reproductive conditions, however, maternal behaviors were not correlated with hormone levels. These results suggest that maternal responsiveness in marmosets may be attenuated during pregnancy, especially late pregnancy, and this may contribute to infanticide by breeding females.     

Tactics of care for young infants by forest-living ruffed lemurs (Varecia variegata variegata): Ground nests,parking, and biparental guarding

Over a 4 month period, systematic and ad libitum observations were conducted on two adult female black-and-white ruffed lemurs (Varecia variegata variegata) and their infants in a 3.5 ha forest enclosure. The females were mother and daughter, members of a family group that had been semifree-ranging for 2 years and 3 months at the time of the births. One to two weeks before parturition, the females independently constructed nests, in which they kept their infants during the first few weeks following parturition. The older mother, cage-reared herself, prepared at least one nest. Her daughter, who has lived in the forest since late juvenescence, prepared at least four. Two to three weeks after parturition, the mothers moved their infants high into trees. During periods of maternal absence, the infants were often alone, and they rarely or never moved, vocalized, or groomed themselves. The mothers often kept their infants together after nests were no longer used. Each infant nursed freely from both lactating females. The infants were carried orally only by their mothers and were never transported by clinging to the pelage of any group members. Previously, researchers suggested that ruffed lemurs build nests for care of infants high up in trees. The present observations, however, suggest that two major modes of neonate care in Varecia exist: serial use of multiple ground nests and “parking” of infants high in trees. Advance preparation of several nest sites, relative lack of large predators, alternate maternal and paternal guarding of infants, infant immobility during absence of mother, and rapid infant development make this tactic of care for neonates plausible.     

Fatal attraction: interest in infants and infant abuse in rhesus macaques.

This study investigated whether infant abuse by female rhesus macaques (Macaca mulatta) is a phenomenon specific to their own offspring or reflects a general tendency to interact negatively with infants. Several aspects of the relationship between maternal behavior, infant handling, and infant harassment were also investigated. Study subjects were 20 group-living rhesus mothers with their infants observed during the first 12 weeks of lactation. The results of this study indicate that abusive mothers are highly attracted to infants in general but that infant abuse is a phenomenon specific to their own offspring. Infant harassment is not an accidental by-product of infant handling or the result of maternal inexperience but it is likely related to reproductive competition among lactating females. Maternal behavior and infant handling may be regulated by similar proximate mechanisms, but probably have different adaptive functions and evolutionary history across the Primate order. Am J Phys Anthropol 110:17-25.     

Social rank and sex-biased maternal investment in captive japanese macaques: behavioural and reproductive data

This study investigated the relationship between social rank and sex-biased maternal investment in captive Japanese macaques (Macaca fuscata) using reproductive and behavioural data. High-ranking mothers showed a significantly male-biased secondary sex ratio, spent more time in contact with and carried male infants for longer than female infants. Low-ranking mothers showed no bias in secondary sex ratio nor in the time spent in contact with male and female infants, but carried female infants for longer. No differences were observed in the interbirth intervals following male and female infants nor in the frequency and intensity of aggression received by mothers with male and female infants, either in high-ranking or in low-ranking mothers. These results show that Japanese macaque mothers can adopt flexible and rank-dependent rearing strategies.     

Behavioral processes and costs of co-existence in female spotted hyenas: a life history perspective

We assessed the importance of three behavioral processes on the fitness of individual females as mediated via maternal care in matrilineally organized social groups of spotted hyenas Crocuta crocuta. These were maternal choice of foraging tactic, the maintenance of individual dominance rank (social status) within the adult female hierarchy, and the behavioral support provided by mothers to their daughters when daughters acquired their position in the adult female hierarchy. The effects of all behavioral processes were closely linked. Maternal care was dependent on maternal social status because high ranking females had priority of access to food, and individual maternal choice of foraging tactic was frequency – and social status-dependent when medium prey abundance provided an opportunity for such a choice. At medium prey abundance, low ranking females went on costly long distance commuting trips to forage on migratory herds outside the group territory, whereas high ranking females fed on kills within the group territory. As a consequence, offspring of high ranking females grew faster, had a higher chance of survival to adulthood, and thus high ranking females had a higher lifetime reproductive success. Daughters of high ranking females usually acquired a social status immediately below that of their mother provided they enjoyed the effective support from their mothers as coalition partners, and they gave birth to their first litter at an earlier age than daughters of low ranking mothers. Spotted hyenas are therefore an example of the silver-spoon effect. This study shows that the frequency-dependent outcome of behavioral processes can be a key determinant of maternal reproductive success in social carnivores and have a profound influence on the reproductive career prospects of offspring.     

Weaning Age,Infant Care,and Behavioral Development in <Emphasis Type="Italic">Trachypithecus leucocephalus</Emphasis>

Primate infants are born in an altricial state and rely on the care of their parents for a relatively long period of time. Parental investment is critical to offspring survival and thus to the reproductive success of the parent as well. However, mothers and infants may experience a conflict of interest, in that infants may benefit by receiving prolonged maternal care but mothers may curtail such care in a tradeoff between investment in current versus future offspring. Documenting life history characteristics, such as age at weaning, is important not only for understanding the conflicts of interest and tradeoffs; such information can also provide insights about female reproductive rates and be valuable for conservation efforts. Little is known about the life history of white-headed langurs (Trachypithecus leucocephalus), despite their endangered status. We were the first to investigate mother-infant relationships and infant behavioral development in the species. We studied 3 wild mother-infant pairs throughout infancy. We used data from >460 h of focal subject sampling to calculate the proportion of time individuals spent in different behavioral states and the frequency of instantaneous events, such as maternal rejection. White-headed langur infants depended on their mothers for 19–21 mo, at which time they were weaned. Maternal rejection facilitated infant independence in the early stages of infant development, and mothers stopped investing in their infants when they resumed estrus. The weaning age of the wild white-headed langurs we studied was dramatically longer than that of captives, possibly as a result of the nutritional differences between wild and captive populations. Weaning age was also longer than for most other Asian colobines, and may be attributable to the degradation and fragmentation of their natural habitat.     

Maternal trade-off in treating high-risk children

Low birthweight and the infant's health status are expected to strongly influence the child's reproductive value and, thus, the maternal decisions on the amount and timing of investment. A total of 590 Hungarian primiparous mothers giving birth in the late 1980s were recruited for the longitudinal study. Mothers of high-risk infants shortened the duration of breast-feeding and interbirth intervals, compared to those with an infant of higher survival prospects. The most powerful predictor of the length of the lactation period was the infant's weight at birth, whereas birth spacing was significantly influenced by the health status of the older child. Socioeconomic status had a positive effect on maternal care as well, but it did not change the basic pattern of diminishing maternal care as a function of the infants' low reproductive value. The combination of the above factors resulted in a cumulative effect on maternal investment of mothers with handicapped children of various degrees of risk. An attempt has been made to exclude alternative explanations and to discuss the proximate mechanisms of discriminative parental solicitude.     

Is There Adaptive Value to Reproductive Termination in Japanese Macaques? A Test of Maternal Investment Hypotheses

Evolutionary biologists often argue that menopause evolved in the human female as the result of selection for a postreproductive phase of life, during which increased maternal investment in existing progeny could lead to enhanced survivorship of descendents. Adaptive theories relating menopause to enhanced maternal investment are known as the mother (first-generation) and grandmother (second-generation-offspring) hypotheses. Although menopause—universal midlife termination of reproduction—has not been documented in primates other than humans, some researchers have argued that postreproductive alloprimates also have a positive impact on the survivorship of first and second generation progeny. We tested the maternal investment hypotheses in Japanese macaques by comparing the survivorship of offspring, final infants, and great-offspring of females that terminated reproduction before death with females that continued to reproduce until death. SURVIVAL analyses revealed no significant difference in the survivorship of descendents of postreproductive and reproductive females, though final infants of postreproductive females were 13% more likely to survive than final infants of females that reproduced until death were. We also explored possible differences between these two groups of females, other than survivorship of progeny. We found no difference in dominance rank, matrilineal affiliation, body weight, infant sex ratio, age at first birth, fecundity rate or lifetime reproductive success. However, postreproductive females are significantly longer-lived than reproductive females and as a result experienced more years of reproduction and produced more infants in total. Apart from final infants, offspring survival is marginally lower in postreproductive females. Since offspring survival is not significantly enhanced in postreproductive females, the greater number of infants produced did not translate into greater lifetime reproductive success. Our findings fail to support the maternal investment hypotheses and instead suggest that reproductive termination in this population of Japanese macaques is most closely associated with enhanced longevity and its repercussions.     

Opportunistic mothers: female marmosets (Callithrix kuhlii) reduce their investment in offspring when they have to, and when they can

All female primates incur energetic costs associated with producing and caring for offspring, but females belonging to the New World primate family Callitrichidae, the marmosets and tamarins, appear to face even further demands. In fact, the energetic demands of rearing callitrichid infants are thought to have led to the evolution of cooperative infant care in these species. If this explanation is true, then one might expect that natural selection should also have shaped patterns of maternal behavior to be sensitive to the costs of reproduction and equipped females to reduce their investment in offspring under certain conditions. Therefore, we examined the maternal effort and postpartum endocrine profiles of individual female marmosets (Callithrix kuhlii) across conditions that represented two hallmarks of callitrichid reproduction-conception during the early postpartum period and alloparental assistance. When females conceived during the early postpartum period and faced the upcoming demands of caring for their newly conceived litters (Study 1), they significantly reduced their caregiving effort and had significantly higher postpartum levels of estradiol relative to breeding attempts in which conception occurred later in the postpartum period. Postpartum estradiol was negatively correlated with maternal carrying effort. When experienced alloparents were present (Study 2), females again reduced their caregiving effort relative to breeding attempts in which experienced alloparents were not present. Postpartum cortisol, however, did not vary as a function of experienced alloparental assistance. The results of these studies suggest that female marmosets have been subjected to similar selection pressures as females of other primate taxa--to maximize their reproductive success by reducing their investment in offspring under the worst and best of conditions--and suggest that hormones may mediate within-female variation in maternal care. These studies also provide support for the notion that mothers are "flexible opportunists" when it comes to providing care to their young.     

No evidence for sex biases in milk macronutrients,energy, or breastfeeding frequency in a sample of filipino mothers

Maternal reproductive investment includes both the energetic costs of gestation and lactation. For most humans, the metabolic costs of lactation will exceed those of gestation. Mothers must balance reproductive investment in any single offspring against future reproductive potential. Among mammals broadly, mothers may differentially invest in offspring based on sex and maternal condition provided such differences investment influence future offspring reproductive success. For humans, there has been considerable debate if there are physiological differences in maternal investment by offspring sex. Two recent studies have suggested that milk composition differs by infant sex, with male infants receiving milk containing higher fat and energy; prior human studies have not reported sex‐based differences in milk composition. This study investigates offspring sex‐based differences in milk macronutrients, milk energy, and nursing frequency (per 24 h) in a sample of 103 Filipino mothers nursing infants less than 18 months of age. We found no differences in milk composition by infant sex. There were no significant differences in milk composition of mothers nursing first‐born versus later‐born sons or daughters or between high‐ and low‐income mothers nursing daughters or sons. Nursing frequency also showed no significant differences by offspring sex, sex by birth order, or sex by maternal economic status. In the Cebu sample, there is no support for sex‐based differences in reproductive investment during lactation as indexed by milk composition or nursing frequency. Further investigation in other populations is necessary to evaluate the potential for sex‐based differences in milk composition among humans. Am J Phys Anthropol 152:209–216, 2013. © 2013 Wiley Periodicals, Inc.     

Maternal Oxytocin Is Linked to Close Mother-Infant Proximity in Grey Seals (Halichoerus grypus)

Maternal behaviour is a crucial component of reproduction in all mammals; however the quality of care that mothers give to infants can vary greatly. It is vital to document variation in maternal behaviour caused by the physiological processes controlling its expression. This underlying physiology should be conserved throughout reproductive events and should be replicated across all individuals of a species; therefore, any correlates to maternal care quality may be present across many individuals or contexts. Oxytocin modulates the initiation and expression of maternal behaviour in mammals; therefore we tested whether maternal plasma oxytocin concentrations correlated to key maternal behaviours in wild grey seals (Halichoerus grypus). Plasma oxytocin concentrations in non-breeding individuals (4.3 ±0.5 pg/ml) were significantly lower than those in mothers with dependent pups in both early (8.2 ±0.8 pg/ml) and late (6.9 ±0.7 pg/ml) lactation. Maternal plasma oxytocin concentrations were not correlated to the amount of nursing prior to sampling, or a mother’s nursing intensity throughout the dependant period. Mothers with high plasma oxytocin concentrations stayed closer to their pups, reducing the likelihood of mother-pup separation during lactation which is credited with causing starvation, the largest cause of pup mortality in grey seals. This is the first study to link endogenous oxytocin concentrations in wild mammalian mothers with any type of maternal behaviour. Oxytocin’s structure and function is widely conserved across mammalian mothers, including humans. Defining the impact the oxytocin system has on maternal behaviour highlights relationships that may occur across many individuals or species, and such behaviours heavily influence infant development and an individual’s lifetime reproductive success.     

Maternal influences on the sexual behavior and reproductive success of the female rat

In many species, including humans, there is evidence for parental effects on within-sex variations in reproductive behavior. In the present studies we found that variations in postnatal maternal care were associated with individual differences in female sexual behavior in the rat. Females born to and reared by dams that showed enhanced pup licking/grooming (i.e., High LG mothers) over the first week postpartum showed significantly reduced sexual receptivity and alterations in the pacing of male mounting (i.e., longer inter-intromission intervals) observed in a paced mating test. There were minimal effects on the sexual behavior of the male offspring. The female offspring of High LG mothers showed a reduced lordosis rating, a decreased mount:intromission ratio, received fewer ejaculations and were less likely to achieve pregnancy following mating in the paced mating context. The data suggest maternal influences on the sexual development of the female rat that are functionally relevant for reproductive success. Together with previous studies these findings imply that maternal care can ‘program’ reproductive strategies in the female rat.     

The evolution of the patterning of human lactation: A comparative perspective

Some four decades ago, Jeanne Altmann started her detailed field studies of baboon mothers and their infants with a focus on the behavioral ecology of maternal reproductive investment. 1 Around the same time, Sarah Hrdy studied langur mothers and their infants, focusing on the influence of the social environment on a female's reproductive options and decisions. 2 Their pioneering work has inspired many subsequent studies of female primate reproduction in its natural context and shaped our own work on primate mothers.     

Effects of hand‐rearing on the reproductive success of western lowland gorillas in North America

This study sought to assess the potential effects of hand‐rearing by evaluating the relationships among rearing type and reproductive success in the American Zoo and Aquarium Association's Species Survival Plan^® for western lowland gorillas. Our study included data on 697 gorillas: 257 wild‐born (WB) and 440 born at zoos or related facilities in North America. We found no significant differences in the number of reproductive zoo‐born (ZB) and WB females, but more WB males sired infants than their ZB counterparts. This was influenced by a skew in the number of reproductive years for WB males in the studbook. ZB males showed no difference in infants produced per reproductive year, as compared to WB males, while ZB females produced more infants per reproductive year than did WB females. Mother‐reared (MR), ZB females produced more offspring and used more reproductive opportunity than hand‐reared (HR) females, whereas rearing had no effect on the reproductive success of ZB males. Moreover, MR and partially hand‐reared (PHR) females were more likely to become nurturing mothers themselves. Zoo Biol 21:389–401, 2002. © 2002 Wiley‐Liss, Inc.