Sex-biased Maternal Investment Research Articles

Maternal Investment Fosters Male but Not Female Social Interactions with Other Group Members in Immature Wild Spider Monkeys (Ateles geoffroyi).

In several species, individuals form long-lasting social relationships with other group members, which provide them with important fitness benefits. In primates, patterns of social relationships are known to differ between sexes, but little is known about how these differences emerge through development or the role that mothers might have in this process. Here, we investigated how sex differences in social behaviour emerge during the first six years of primate life and how sex-biased maternal investment can foster immatures' social development and social interaction with other group members. For this purpose, we observed 20 males and females aged between zero and six years in a wild group of spider monkeys (Ateles geoffroyi) that was male-philopatric and, therefore, expected to show sex-biased maternal investment. Our results showed no sex difference in the social development of offspring with regards to body contact and grooming, but the probability of play was rather constant throughout age for females, whereas, for males, it became higher than females around two years of age, peaking between three and four years of age. Moreover, we found differences between female and male immatures in the importance of maternal investment (which included the time mothers spent nursing, carrying, grooming, touching and playing with their offspring) for their social integration in the natal group. In particular, maternal investment increased the probability of playing with other group members for sons, but not for daughters. Our findings suggest that mothers, through sex-biased maternal investment, might have a crucial function in the social development of spider monkeys, fostering the abilities that young offspring need to thrive as adults. By shedding light on maternal investment and social development in a still understudied primate species, these findings contribute to understanding the evolutionary roots of human maternal care and social development.

Sex-specific effects of the in ovo environment on early-life phenotypes in eiders

Maternal effects affect offspring phenotype and fitness. However, the roles of offspring sex-specific sensitivity to maternal glucocorticoids and sex-biased maternal investment remain unclear. It is also uncertain whether telomere length (a marker associated with lifespan) depends on early growth in a sex-specific manner. We assessed whether maternal traits including corticosterone (CORT; the main avian glucocorticoid) and in ovo growth rate are sex-specifically related to offspring CORT exposure, relative telomere length (RTL) and body condition in eiders (Somateria mollissima). We measured feather CORT (fCORT), RTL and body condition of newly hatched ducklings, and growth rate in ovo was expressed as tarsus length at hatching per incubation duration. Maternal traits included baseline plasma CORT, RTL, body condition and breeding experience. We found that fCORT was negatively associated with growth rate in daughters, while it showed a positive association in sons. Lower offspring fCORT was associated with higher maternal baseline plasma CORT, and fCORT was higher in larger clutches and in those hatching later. The RTL of daughters was negatively associated with maternal RTL, whereas that of males was nearly independent of maternal RTL. Higher fCORT in ovo was associated with longer RTL at hatching in both sexes. Duckling body condition was mainly explained by egg weight, and sons had a slightly lower body condition. Our correlational results suggest that maternal effects may have heterogeneous and even diametrically opposed effects between the sexes during early development. Our findings also challenge the view that prenatal CORT exposure is invariably associated with shorter telomeres.

Mismatched Prenatal and Postnatal Maternal Depressive Symptoms and Child Behaviours: A Sex-Dependent Role for NR3C1 DNA Methylation in the Wirral Child Health and Development Study

Evolutionary hypotheses predict that male fetuses are more vulnerable to poor maternal conditions (Sex-biased Maternal Investment), but female fetuses are at greater risk of glucocorticoid-mediated disorders where there is a mismatch between fetal and postnatal environments (Predictive Adaptive Response). Self-reported prenatal and postnatal depression and maternal report of child anxious-depressed symptoms at 2.5, 3.5 and 5.0 years were obtained from an ‘extensive’ sample of first-time mothers (N = 794). Salivary NR3C1 1-F promoter methylation was assayed at 14 months in an ‘intensive’ subsample (n = 176) and stratified by psychosocial risk. Generalised structural equation models were fitted and estimated by maximum likelihood to allow the inclusion of participants from both intensive and extensive samples. Postnatal depression was associated with NR3C1 methylation and anxious-depressed symptoms in daughters of mothers with low prenatal depression (prenatal-postnatal depression interaction for methylation, p < 0.001; for child symptoms, p = 0.011). In girls, NR3C1 methylation mediated the association between maternal depression and child anxious-depressed symptoms. The effects were greater in girls than boys: the test of sex differences in the effect of the prenatal-postnatal depression interaction on both outcomes gave X2 (2) = 5.95 (p = 0.051). This was the first human study to show that epigenetic and early behavioural outcomes may arise through different mechanisms in males and females.

Different maternal investment strategies for male and female calves in a polygynous mammal.

Maternal effects occur when the phenotype of the mother influences that of the young to the detriment of her survival, growth or fitness. The investment of the mother can be affected by maternal body condition and/or experience. Trivers–Willard Hypothesis (TWH) and Local Resource Competition Hypothesis (LRCH) are the main hypotheses used to explain bias in birth sex-ratios in mammals, as well as for sex-biased maternal investment. Both hypotheses suggest that a different amount of investment must be expected according to the sex of the young. However, recent studies suggest that these differences are not in quantity but in the strategies: mechanisms and objectives may differ for each sex. We studied how maternal characteristics (age, body mass, body condition, and dominance status) influence relevant aspects of the birth and early growth of the calf (birth date, birth body mass, body mass at weaning, and body condition at weaning) separately for each sex; and how that investment is mediated by milk production and composition (lactose, fat, and protein). One hundred eighty-eight newborns from 75 captive red deer hinds aged from 2 to 19 years were analyzed. The main differential investment observed was related to birth date: when producing a female, hinds give birth earlier in the season only if they have a good body condition; however, when gestating a male it is the older hinds those which deliver earlier. Subsequently, milk production and composition are correlated with birth body mass in female calves, but to weaning body mass in males. Thus, only hind body mass affects the weaning body mass of female calves, compared with age and hind body mass in males. These results suggest that while TWH fits the maternal investment strategy found for male calves, it is LRCH which correlates with the maternal investment patterns observed for females.

Influence of social dominance on the secondary sex ratio and factors affecting hierarchy in Holstein dairy cows

In several studies of different species, the proportions of male and female offspring did not match the statistical assumption of 50:50. Aside from environmental and genetic factors, biological parameters were found to influence the sex ratio. Three hypotheses (Trivers-Willard, advantaged daughter, and the local resource competition hypothesis) have been proposed, stating that the sex of progeny might be influenced by sex-biased maternal investment in the raising of offspring. The results of existing studies are still conflicting, even within studies on the same species. The aim of the present study was to investigate whether the dominance status of cows influences the secondary sex ratio. A herd of lactating cows was observed directly for 126h, and a dominance index (DI) was established for 71 individuals (aged between 2.6 and 9.8 yr) for which at least 8 encounters had been observed to categorize individuals as subordinate, intermediate, or dominant. Furthermore, the number and sex of calves were assessed, and further individual characteristics of the animals (e.g., age, milk yield, body condition, and lameness scores) were analyzed for interrelationships with dominance status as well as the influence of the DI on the secondary sex ratio. The results indicated that the DI was independent of age, but a negative correlation was found between DI and lameness, whereas a positive correlation was shown for DI and body condition score. In general, more dominant animals had lower lameness scores and better body conditions. No sex ratio bias was found for primi- or for pluriparous animals and no seasonal influences were detected. The proportion of male offspring was significantly correlated with the DI of lactating cows, where animals with a higher social rank produced a lower proportion of male progeny. The pairwise comparison between dominant and subordinate lactating cows revealed a significant difference in the sex ratios of progeny, with subordinate animals having more male calves. These results indicate that the maternal dominance rank was associated with the secondary sex ratio in cattle. These observations are generally in agreement with the advantaged daughter hypothesis.

Lack of Sex-Biased Maternal Investment in spite of a Skewed Birth Sex Ratio in White-Headed Langurs (Trachypithecus leucocephalus)

Numerous hypotheses have been developed to explain sex allocation. In male-dispersing, female cooperatively breeding species, the local resource competition model predicts male-biased birth sex ratio, the local resource enhancement model predicts female-biased birth sex ratio, and the population adjustment model predicts that biased birth sex ratio should not be favored if the two sexes are equally costly to rear. The male quality model predicts that, in polygynous species, females in better physical condition will either produce more sons than daughters or invest more heavily in sons than in daughters. White-headed langurs are a female philopatry and female cooperatively breeding species. During a 11-yr study, a total of 133 births were recorded, among which birth sex ratio (M:F = 73:49) was significantly male-biased. This is consistent with the prediction of the local resource competition model. On the other hand, if mothers balanced their investment between the two sexes, according to Fisher’s population adjustment model, males should be the less-costly-to-rear sex. However, we found no sex difference for infant mortality (12.3% in males and 12.2% in females), and sons induced slightly longer interbirth interval (son: 26.4 ± 1.1 mo, daughter: 24.1 ± 0.6 mo) and lactational period (son: 20.9 ± 1.0 mo, daughters: 19.6 ± 0.5 mo) for their mothers. Thus, the population adjustment model was not supported by this study. The local resource enhancement model was not supported because birth sex ratio did not bias to females who provided more reproductive assistance. On the individual level, probit regression showed no relation between birth sex ratio and group size. Because the group size was considered to be negatively related to female physical condition, our study did not support the male-quality model. We suggested several possibilities to explain these results.

Life history correlates of inbreeding depression in mandrills (Mandrillus sphinx)

Inbreeding depression reflects the negative consequences of increased homozygosity at genes that affect fitness. We investigate inbreeding depression in a semi-free-ranging colony of mandrills (Mandrillus sphinx), using high-quality pedigree data, comprising five maternal generations and 20 years of morphological and demographic data. We examine the relationship between inbreeding coefficients and four fitness correlates: two growth parameters (mass and height for age) and longevity in both sexes, and age at first conception in females. Inbreeding was correlated with both growth parameters, but only in females, with inbred females being smaller than noninbred females. Inbreeding was also correlated significantly with age at first conception, with inbred females giving birth earlier in life than noninbred females. We suggest that sex-biased maternal investment may explain this sex-differential response to inbreeding, although the lack of a significant association between inbreeding and growth in males may also be due to the provisioned nature of the colony. The surprising relationship between age at first conception and inbreeding may be related to smaller adult size in inbred females, or to their being less able to escape from male sexual coercion.

Mother-calf relationships and maternal investment in European bisonBison bonasus

Mother-young relationships, up to the third month of the calves’ life, were investigated in European bisonBison bonasus (Linnaeus, 1758) from Białowieża National Park breeding centres (Poland). During the first week, calves spent most of their time close to their mothers and were rarely seen in the vicinity of other group members. Highest suckling rate, most frequent vocal contact and agonistic behaviour of mothers towards intruders, were other characteristics of this period. Although being a forest species, European bison exhibit a following type of strategy for offspring protection, typical for ungulates living in open areas; no hiding phase was observed. Suckling rates were similar in calves of both sexes, however, the pattern of nursing was different: male calves suckled longer, but in rarer bouts than female calves. The mothers’ condition, reflected by their social rank, did not influence the suckling rate. No sex differences were recorded in other maternal activities or mother-calf distance. The presumption of a lack of sex-biased maternal investment in European bison is confirmed by the results of other research.

Maternal Investment in Captive Giraffes

Sex-biased maternal investment involves differential allocation of resources to production and rearing of sons or daughters as a function of their anticipated reproductive output. We examined reproductive investment among captive giraffes (Giraffa camelopardalis) over a 21-year period to determine extent to which females invest differentially in offspring by sex. We found an unbiased sex ratio at birth and comparable interbirth intervals following rearing of either sons or daughters. Early neonatal mortality compressed interbirth interval and females probably conceived while lactating. We suggest that females invest equally in sons and daughters because males surpass females in size subsequent to the period of infant dependency.

MATERNAL INVESTMENT IN CAPTIVE GIRAFFES

Sex-biased maternal investment involves differential allocation of resources to production and rearing of sons or daughters as a function of their anticipated reproductive output. We examined reproductive investment among captive giraffes (Giraffa camelopardalis) over a 21-year period to determine extent to which females invest differentially in offspring by sex. We found an unbiased sex ratio at birth and comparable interbirth intervals following rearing of either sons or daughters. Early neonatal mortality compressed interbirth interval and females probably conceived while lactating. We suggest that females invest equally in sons and daughters because males surpass females in size subsequent to the period of infant dependency.

MATERNAL DOMINANCE RANK AND AGE AFFECT OFFSPRING SEX RATIO IN PIGTAIL MACAQUES

This study tested some predictions of the local-resource-competition hypothesis and localresource-enhancement hypothesis of sex-biased maternal investment in a population of pigtail macaques (Macaca nemestrina leonina). Offspring sex ratios in high- and lowranking matrilines were biased in opposite directions as predicted. Sex ratio in the middleranking matriline was female biased similar to the high-ranking matrilines but became increasingly male biased with maternal age, similar to the low-ranking matrilines. Interbirth intervals following surviving daughters were longer than those following sons, irrespective of rank, suggesting that daughters were more costly to rear than sons. Infant mortality was not significantly different for sons and daughters. The findings of this study are consistent with some, but not all, of the predictions of local-resource-competition and local-resourceenhancement hypotheses and suggest that middle-ranking mothers have specific investment strategies that change in relation to their age.

Variation of male‐biased maternal investment in fallow deer ( Dama dama )

In this study 529 fallow deer fawns were captured and weighed at Donana National Park, Spain. An annual index of male-biased maternal investment (MBMI) was calculated, and this index was found to vary in relation to environmental factors. Thus, the level of MBMI was sensitive to fluctuations of autumn rainfall and the male-biased maternal investment carried out by mothers in the previous year (MBMIP). Our results reveal that those factors related to the female's body condition at the beginning of gestation have a high contribution to the variation of differential pre-natal maternal investment. It has been hypothesized by other authors that male-biased maternal investment is limited by the level of total maternal expenditure and these authors classified the fallow deer as a species near to its maximum reproductive effort, in which no sex-biased maternal investment exists. Our study reveals that male-biased maternal investment in fallow deer does exist and supports the hypothesis that sensitivity of maternal investment to environmental conditions could be expected to occur in species with high reproductive effort and sex-biased maternal investment.

Sex allocation in a polygynous mammal with large litters: the wild boar

Predictions from Trivers & Willard's (1973, Science, 179, 90–92) hypothesis of sex-biased maternal investment in polygynous species do not apply well to species where mothers produce more than one offspring per reproductive attempt. First, as litter size increases, the benefits to the mother of adjusting sex ratio decrease because (1) she could benefit more by adjusting litter size and (2) sex differences in reproductive potential are negatively related to litter size. Second, testing sex-biased investment in these species requires predictions about the simultaneous adjustment of sex ratio and litter size. The wild boar, Sus scrofa, although polygynous, produces large litters. Here we present data for 58 litters from a free-ranging wild boar population in central Spain. Maternal expenditure per individual offspring, as measured by piglet weight, was higher for male than female fetuses. In more than 81% of cases the heaviest fetus in the litter was a male regardless of the quality of the mother; this might have influenced his ranking within the ‘teat order’ and consequently his development and survival. Mother quality (size and weight) appeared to be related to litter size but not to the sex ratio of the litter. However, it was highly related to a variable that combined the effects of litter size and sex ratio within the litter, thus supporting Williams' (1979, Proceedings of the Royal Society of London, Series B, 205, 567–580) hypothesis that mothers should adjust both litter size and offspring sex.

Tactics of Maternal Investment of Northern Grasshopper Mice in Response to Postnatal Restriction of Food

Various theories predict sex-biased maternal investment under specific environmental or maternal conditions. The Trivers-Willard hypothesis, for instance, predicts that in some polygynous species maternal investment should be biased toward daughters when the mother is in poor condition. Empirical data testing this hypothesis are equivocal. I compared patterns of maternal investment in lactating northern grasshopper mice ( Onychomys leucogaster ) allowed unrestricted access to food with those of mothers that received 80% of requirements for non-lactating mice. Nutritionally deprived mothers either attempted to rear their entire litter, or killed and consumed all young before maternal mass dropped below 75% of initial mass. Growth rates of young from experimental litters were lower than those from control litters, but there was no evidence of sex-biased maternal investment.

Effects of maternal nutrition on post-weaning growth in two North American rodents

The Trivers-Willard hypothesis of sex-biased maternal investment in response to fluctuations in resource availability has provided a theoretical foundation for research on maternal investment for more than two decades. Their hypothesis holds that mothers in poor condition as a result of poor resource availability should bias parental investment towards offspring with the highest probability of reproducing. In the polygynous mating system of mammals where males compete for breeding access to females, the hypothesis predicts investment favoring females. Although data from many systems have supported this hypothesis, other systems do not follow the predicted patterns and have resulted in various alternative hypotheses. The present research was designed to test whether differences in body condition of young reared by nutritionally stressed dams relative to young reared by unstressed dams were maintained into adulthood, one of the fundamental assumptions underlying the Trivers-Willard hypothesis. Post-weaning growth in eastern woodrats (Neotoma floridana) and northern grasshopper mice (Onychomys leucogaster) was examined relative to maternal nutritional plane. Individuals from undernourished dams were lighter than their unrestricted counterparts at weaning but no difference was evident by the time they had reached adult size. Failure to maintain body condition differences into adulthood violates one of the assumptions essential for application of the Trivers-Willard hypothesis of maternal investment patterns. Although the Trivers-Willard model proposed that natural selection favors differential investment in the sexes over the entire course of parental investment, evidence from this and other studies suggests that the Trivers-Willard hypothesis might not be appropriate to address maternal investment questions in postnatally malnourished dams, but instead should be restricted to systems concerned with prenatal maternal condition or resource availability.

Maternal response to resource limitations in eastern woodrats

Prevailing theories concerning maternal investment strategies to maximize fitness under adverse environmental conditions predict sex-biased investment in offspring under certain circumstances. These predictions have received empirical support in some species but not in others. The present study was designed to assess patterns of maternal investment in postnatally food-restricted eastern woodrats, Neotoma floridana, in an attempt to replicate previous work and to examine patterns of resource allocation in greater detail. Experimental dams received a food ration that supplied approximately 80% of non-lactating nutritional requirements, whereas control dams had unrestricted access to food. To limit the level of stress experienced by lactating mothers, individual females were allowed unlimited access to food for the duration of the lactation period if their mass fell below 75% of their pre-experimental mass. Food restricted dams attempted to rear all offspring despite experiencing considerable weight loss themselves. Growth rates of young from experimental litters were significantly lower than those of young from control litters. In contrast to previously reported data, no evidence of sex-biased maternal investment was found in this species.

Further evidence of sex-biased maternal investment by Mongolian gerbil dams

There is theoretical reason to expect that ill--PDlygynous species, as a consequence of competition between males for access to females, (I) a given increment in parental investment (Trivers 1972) will have a greater effect on the fitness of males than of females and (2) parents will make greater investment in individual sons than in individual daughters (Trivers & Willard 1973;Clutton-Brock & Albon 1982;Clutton-Brock & lason 1986). Unfortunately, as Clutton-Brock & Albon (1982), Clutton-Brock & lason (1986) and Hrdy (1987) each have made clear, in their respective reviews of relevant literature, predictions about sexbiased parental investment are difficult to test empirically because of the lack of data describing either the fitness costs to parents of rearing young of each sex or the relative effects of a given amount of parental investment on the survival and reproduction of offspring of each sex. In a recent paper (Clark et al. 1990),we presented evidence that female Mongolian gerbils, Meriones unguiculatus, exhibit a greater loss in reproductive potential after rearing sons than after rearing daughters. Here, we examine effects of reductions in maternal investment on rates of growth of nursing male and female Mongolian gerbil pups. On theoretical grounds (Clutton-Brock & lason 1986), one would expect male pups to be more vulnerable to parental deprivation than their sisters. Our subjects were 41 litters of gerbils, born to primiparous females descended from breeding stock acquired from Tumblebrook Farms (Brookfield, Massachusetts). On the day of birth, each litter was culled to two male and two female pups and each pup was toe clipped for individual recognition. Because of the demands of our experimental design, we used only those 30 litters that, on day 5 postpartum, had all four pups both alive and (to exclude runts) within a range of 0,5 g in weight. Three female and two male pups, one in each of five litters, died between days I and 5 postpartum. On day 5 postpartum, we randomly assigned each litter to one of three groups (10 litters/group) that experienced either 0, 2 or 4 h/day of separation

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.