Persistence of maternal effects in baboons: Mother's dominance rank at son's conception predicts stress hormone levels in subadult males

Dominance status and reproductive experience are maternal characteristics that affect offspring traits in diverse taxa, including some cercopithecine primates. Maternal effects of this sort are widespread and are sources of variability in offspring fitness. We tested the hypothesis that maternal dominance rank and reproductive experience as well as a male's own age and dominance rank predicted chronic fecal glucocorticoid (fGC) concentrations in 17 subadult wild male baboons, Papio cynocephalus (median age 6.5 years), in the Amboseli basin, Kenya. Among these variables, maternal dominance rank at a subadult male's conception was the sole significant predictor of the male's fGC and accounted for 42% of fGC variance; sons of lower ranking mothers had higher fGC than did those of high-ranking mothers. This result is striking because subadult male baboons are approximately 4-6 years past the period of infant dependence on their mothers, and are larger than and dominant to all adult females. In addition, many males of this age have survived their mothers' death. Consequently, the influence of maternal dominance rank persisted well beyond the stage at which direct maternal influence on sons is likely. Persistence of these major maternal influences from the perinatal period may signal organizational effects of mothers on sons' HPA axis. Although short-term, acute, elevations in GC are part of adaptive responses to challenges such as predators and other emergencies, chronically elevated GC are often associated with stress-related pathologies and, thereby, adverse effects on fitness components.     

Relationships of vervet mothers with sons and daughters from one through three years of age

Social relationships between mothers and juvenile offspring were examined in captive, socially-living vervet monkeys (Cercopithecus aethiops sabaeus) to assess the effects of offspring age and sex, and the mother's dominance rank on behavioural interactions. The results indicate that both high-and low-ranking mothers approach and groom their daughters more than they approach and groom their sons. The frequency of both aggressive behaviour toward offspring and support of offspring in agonistic encounters with other group members is influenced by the mother's dominance rank, but not by offsprin sex. Compared to sons, daughters (particularly daughters of high-ranking females) approach and groom their mothers more often, and support their mothers more often in intra-group aggression. The results are discussed in terms of several predictions from parental investment theory and the concept of mutualism.     

Great expectations: dominance,breeding success and offspring sex ratios in red deer

Differences in dominance rank among red deer (Cervus elaphus) females (hinds) on Rhum were related to their breeding success as well as to the comparative success of male and female offspring. Males (stags) born to mothers above median rank were more successful than hinds, while hinds born to subordinate mothers were more successful than stags. The ratio of male to female calves produced by dominant mothers was significantly higher than that produced by subordinates. Since dominance rank among hinds is related to their body weight as adults and to their birth weight, these results suggest that the birth sex ratio may be affected by environmental factors operating during a female's early development.     

Competition among female long-tailed macaques,Macaca fascicularis

In species with permanent groups, the groups tend to move toward a size where competition for food regulates female fitness. Hence, one would expect females to use behavioural means to gain a reproductive advantage over other females in the group. Their competitive ability is likely to reflect dominance rank and age. Adult female Sumatran long-tailed macaques, Macaca fascicularis, in four different groups were studied. Females of a higher dominance rank had a total food intake equal to or higher than that of the lower-ranking females, acquired it at a lower energy cost and probably ate food of higher quality. The older and lower-ranking females avoided competition by more often moving away from the centre of the group. Mortality fell more heavily on females who were less frequently present in the main party. High-ranking females tended to produce more offspring surviving to 1-year, with top-ranking females tending to out-reproduce all others. It is concluded that safety monopolization was the predominant mode of competition among the females caused by the monopolization of clumped food within the main party by high-ranking females.     

Unrelated Helpers in a Primitively Eusocial Wasp: Is Helping Tailored Towards Direct Fitness?

The paper wasp Polistes dominulus is unique among the social insects in that nearly one-third of co-foundresses are completely unrelated to the dominant individual whose offspring they help to rear and yet reproductive skew is high. These unrelated subordinates stand to gain direct fitness through nest inheritance, raising the question of whether their behaviour is adaptively tailored towards maximizing inheritance prospects. Unusually, in this species, a wealth of theory and empirical data allows us to predict how unrelated subordinates should behave. Based on these predictions, here we compare helping in subordinates that are unrelated or related to the dominant wasp across an extensive range of field-based behavioural contexts. We find no differences in foraging effort, defense behaviour, aggression or inheritance rank between unrelated helpers and their related counterparts. Our study provides no evidence, across a number of behavioural scenarios, that the behaviour of unrelated subordinates is adaptively modified to promote direct fitness interests.     

The benefits of social capital: close social bonds among female baboons enhance offspring survival

Sociality has evolved in many animal taxa, but primates are unusual because they establish highly differentiated bonds with other group members. Such bonds are particularly pronounced among females in species like baboons, with female philopatry and male dispersal. These relationships seem to confer a number of short-term benefits on females, and sociality enhances infant survival in some populations. However, the long-term consequences of social bonds among adult females have not been well established. Here we provide the first direct evidence that social relationships among female baboons convey fitness benefits. In a group of free-ranging baboons, Papio cynocephalus ursinus, the offspring of females who formed strong social bonds with other females lived significantly longer than the offspring of females who formed weaker social bonds. These survival benefits were independent of maternal dominance rank and number of kin and extended into offspring adulthood. In particular, females who formed stronger bonds with their mothers and adult daughters experienced higher offspring survival rates than females who formed weaker bonds. For females lacking mothers or adult daughters, offspring survival was closely linked to bonds between maternal sisters. These results parallel those from human studies, which show that greater social integration is generally associated with reduced mortality and better physical and mental health, particularly for women.     

Are olfactory cues involved in nest recognition in two social species of estrildid finches?

Reliably recognizing their own nest provides parents with a necessary skill to invest time and resources efficiently in raising their offspring and thereby maximising their own reproductive success. Studies investigating nest recognition in adult birds have focused mainly on visual cues of the nest or the nest site and acoustic cues of the nestlings. To determine whether adult songbirds also use olfaction for nest recognition, we investigated the use of olfactory nest cues for two estrildid finch species, zebra finches (Taeniopygia guttata) and Bengalese finches (Lonchura striata var. domestica) during the nestling and fledgling phase of their offspring. We found similar behavioural responses to nest odours in both songbird species. Females preferred the odour of their own nest over a control and avoided the foreign conspecific nest scent over a control during the nestling phase of their offspring, but when given the own odour and the foreign conspecific odour simultaneously we did not find a preference for the own nest odour. Males of both species did not show any preferences at all. The behavioural reaction to any nest odour decreased after fledging of the offspring. Our results show that only females show a behavioural response to olfactory nest cues, indicating that the use of olfactory cues for nest recognition seems to be sex-specific and dependent on the developmental stage of the offspring. Although estrildid finches are known to use visual and acoustic cues for nest recognition, the similar behavioural pattern of both species indicates that at least females gain additional information by olfactory nest cues during the nestling phase of their offspring. Thus olfactory cues might be important in general, even in situations in which visual and acoustic cues are known to be sufficient.     

Contrasting the Effects of Maternal and Behavioral Characteristics on Fawn Birth Mass in White-Tailed Deer

Maternal care influences offspring quality and can improve a mother’s inclusive fitness. However, improved fitness may only occur when offspring quality (i.e., offspring birth mass) persists throughout life and enhances survival and/or reproductive success. Although maternal body mass, age, and social rank have been shown to influence offspring birth mass, the inter-dependence among these variables makes identifying causation problematic. We established that fawn birth mass was related to adult body mass for captive male and female white-tailed deer (Odocoileus virginianus), thus maternal care should improve offspring fitness. We then used path analysis to identify which maternal characteristic(s) most influenced fawn birth mass of captive female white-tailed deer. Maternal age, body mass and social rank had varying effects on fawn birth mass. Maternal body mass displayed the strongest direct effect on fawn birth mass, followed by maternal age and social rank. Maternal body mass had a greater effect on social rank than age. The direct path between social rank and fawn birth mass may indicate dominance as an underlying mechanism. Our results suggest that heavier mothers could use dominance to improve access to resources, resulting in increased fitness through production of heavier offspring.     

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.     

Facultative Sex Allocation and Sex‐Specific Offspring Survival in Barrow's Goldeneyes

Sex allocation theory predicts that females should bias their reproductive investment towards the sex generating the greatest fitness returns. The fitness of male offspring is often more dependent upon maternal investment, and therefore, high‐quality mothers should invest in sons. However, the local resource competition hypothesis postulates that when offspring quality is determined by maternal quality or when nest site and maternal quality are related, high‐quality females should invest in the philopatric sex. Waterfowl – showing male‐biased size dimorphism but female‐biased philopatry – are ideal for differentiating between these alternatives. We utilized molecular sexing methods and high‐resolution maternity tests to study the occurrence and fitness consequences of facultative sex allocation in Barrow's goldeneyes (Bucephala islandica). We determined how female structural size, body condition, nest‐site safety and timing of reproduction affected sex allocation and offspring survival. We found that the overall sex ratio was unbiased, but in line with the local resource competition hypothesis, larger females produced female‐biased broods and their broods survived better than those of smaller females. This bias occurred despite male offspring being larger and tending to have lower post‐hatching survival. The species shows strong female breeding territoriality, so the benefit of inheriting maternal quality by philopatric daughters may exceed the potential mating benefit for sons of high‐quality females.     

Age,reproductive value,and dominance-related behaviour in vervet monkey females: cross-generational influences on social relationships and reproduction

Behavioural interactions among captive socially-living adult female vervet monkeys were analysed to determine whether (1) the motivation to maintain and increase, dominance rank declines with age as individual reproductive value declines, or (2) the cross-generational inheritance of dominance rank causes adult females to continue to involve themselves in dominance-related behaviours for the benefit of their daughters, even though their own reproductive value, is declining. The results indicate that adult females do not reduce their involvement in aggressive and dominance-related behaviours as they age. There was strong support for the hypothesis that older adult females maintain affiliative and supportive ties with their adult daughters, and that the daughters benefit from this relationship both in terms of social relationships and reproductive success. Young adult females without mothers were the recipients of more aggression, were less likely to be defeded when they were attacked and were less likely to challenge the rank of others compared to females with mothers living in the group. Young adult females with mothers produced significantly more surviving offspring and had a lower level of infant mortality than comparable adult females without mothers.     

Dominance and queen succession in captive colonies of the eusocial naked mole-rat,Heterocephalus glaber.

Naked mole-rat colonies exhibit a high reproductive skew, breeding being typically restricted to one female (the ''queen'') and one to three males. Other colony members are reproductively suppressed, although this suppression can be reversed following the removal or death of the queen. We examined dominance and queen succession within captive colonies to investigate the relationship between urinary testosterone and cortisol, dominance rank and reproductive status; and to determine if behavioural and/or physiological parameters can be used as predictors of queen succession. Social structure was characterized by a linear dominance hierarchy before and after queen removal. Prior to queen removal, dominance rank was negatively correlated with body weight and urinary testosterone and cortisol titres in males and females. Queen removal results in social instability and aggression between high ranking individuals. Dominance rank appears to be a good predictor of reproductive status: queens are the highest ranking colony females and are succeeded by the next highest ranking females. The intense dominance-related aggression that accompanies reproductive succession in naked mole-rats provides empirical support for optimal skew theory.     

The role of young guards inXylocopa pubescens

Summary Xylocopa pubescens is a facultatively social species in which two types of guards can be found: 1) old, formerly reproductive guards and 2) young, pre-reproductive guards that usually guard the nest in which they emerged. In this species it is always the dominant female that forages and lays the eggs.This paper focuses on the young females' reasons for guarding. Young guards are characteristically the first females of an emerging brood. They start guarding at an age of 6 days, and continue to do so for on average 10 days, when they start a dominance contest. In comparison to other emerging bees, guards did not receive any more of the incoming food. The presence of young females in the nest was sufficient to deter pollen robbers; the protection was not ameliorated by guarding. Guards did not protect the nest from usurpation by intruding females. The presence of a young guard positively influenced both the number and the duration of foraging flights.All guards attempted to take over dominance inside the nest by fighting with the dominant female. Guards had a probability of 50% of winning this contest, which was distinctly higher than their probability of finding a nest elsewhere. The dominant female was not in all cases the mother of the guard. Therefore, the average increase of indirect fitness by guarding was lower than the expected direct fitness returns from leaving the nest earlier. We therefore conclude that guarding females are environmentally disabled, hopeful reproductives. They may be guarding to determine the right time to risk a fight about dominance and to increase their direct fitness if their attempt to supersede is successful.     

Environmental mismatch results in emergence of cooperative behavior in a passerine bird

A major problem in the evolution of maternal effects is explaining the origin and persistence of maternally induced phenotypes that lower offspring fitness. Recent work focuses on the relative importance of maternal and offspring selective environments and the mismatch between them. However, an alternative approach is to directly study the origin and performance of offspring phenotypes resulting from mismatch. Here, we capitalize on a detailed understanding of the ecological contexts that provide both the cue and the functional context for expression of maternally induced offspring phenotypes to investigate the consequences of environmental mismatch. In western bluebirds, adaptive integration of offspring dispersal and aggression is induced by maternal competition over nest cavities. When nest cavities are locally abundant, mothers produce nonaggressive offspring that remain in their natal population, and when nest cavities are scarce, mothers produce aggressive dispersers. However, a few offspring neither disperse nor breed locally, instead helping at their parent’s nest, and as a result these offspring have unusually low fitness. Here, we investigate whether females produce helpers to increase their own fitness, or whether helpers result from a mismatch between the cues mothers experience during offspring production and the breeding environment that helpers later encounter. We found that producing helpers does not enhance maternal fitness. Instead, we show that helpers, which were the least aggressive of all returning sons in the population, were most common when population density increased from the time sons were produced to the time of their reproductive maturity, suggesting that the helper phenotype emerges when cues of resource competition during offspring development do not match the actual level of competition that offspring experience. Thus, environmental mismatch might explain the puzzling persistence of maternally induced phenotypes that decrease offspring fitness.     

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

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

Mothers matter! Maternal support,dominance status and mating success in male bonobos (Pan paniscus)

Variation in male mating success is often related to rank differences. Males who are unable to monopolize oestrous females alone may engage in coalitions, thus enhancing their mating success. While studies on chimpanzees and dolphins suggest that coalitions are independent of kinship, information from female philopatric species shows the importance of kin support, especially from mothers, on the reproductive success of females. Therefore, one might expect a similar effect on sons in male philopatric species. We evaluate mating success determinants in male bonobos using data from nine male individuals from a wild population. Results reveal a steep, linear male dominance hierarchy and a positive correlation between dominance status and mating success. In addition to rank, the presence of mothers enhances the mating success of sons and reduces the proportion of matings by the highest ranking male. Mothers and sons have high association rates and mothers provide agonistic aid to sons in conflicts with other males. As bonobos are male-philopatric and adult females occupy high dominance status, maternal support extends into adulthood and females have the leverage to intervene in male conflicts. The absence of female support to unrelated males suggests that mothers gain indirect fitness benefits by supporting their sons.     

The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques,Macaca fascicularis

Demographic changes were recorded throughout a 12-year period for three social groups ofMacaca fascicularis in a natural population at Ketambe (Sumatra, Indonesia). We examined the prediction that females' lifetime reproductive success depended on dominance rank and group size. Average birth rate was 0.53 (184 infants born during 349 female years). For mature females (aged 8–20 yr) birth rate reflected physical condition, being higher in years with high food availability and lower in the year following the production of a surviving infant. High-ranking females were significantly more likely than low-ranking ones to give birth again when they did have a surviving offspring born the year before (0.50 vs 0.26), especially in years with relatively low food availability (0.37 vs 0.10). Controlled comparisons of groups at different sizes indicate a decline in birth rate with rroup size only once a group has exceeded a certain size. The dominance effect on birth rate tended to be strongest in large groups. Survival of infants was rank-dependent, but the survival of juveniles was not. There was a trend for offspring survival to be lower in large groups than in mid-sized or small groups. However, rank and group size interacted, in that rank effects on offspring survival were strongest in large groups. High-ranking females were less likely to die themselves during their top-reproductive years, and thus on average had longer reproductive careers. We estimated female lifetime reproductive success based on calculated age-specific birth rates and survival rates. The effects of rank and group size (contest and scramble) on birth rate, offspring survival, age of first reproduction for daughters, and length of reproductive career, while not each consistently statistically significant, added up to substantial effects on estimated lifetime reproductive success. The group size effects explain why large groups tend to split permanently. Since females are philopatric in this species, and daughters achieve dominance rank positions similar to their mother, a close correlation is suggested between the lifetime reproductive success of mothers and daughters. For sons, too, maternal dominance affected their reproductive success: high-born males were more likely to become top-dominant (in another group). These data support the idea that natural selection has favored the evolution of a nepotistic rank system in this species, even if the annual benefits of dominance are small.     

Correlates and Consequences of Dominance in a Social Rodent

In harem‐polygynous societies, body condition is often correlated with dominance rank. However, the consequences of dominance are less clear. High‐ranking males do not inevitably have the highest reproductive success, especially in systems where females mate with multiple males. In such societies, we expect male reproductive success to be more highly skewed than female reproductive success, but reproductive skew in females can still arise from rankings established within matrilineal societies. Dominance can also impact life‐history decisions by influencing dispersal patterns in yearlings. To better understand the function of dominance in harem‐polygynous societies, we studied the causes and consequences of dominance in yellow‐bellied marmots (Marmota flaviventris), a social rodent with skewed male reproductive success and female reproductive suppression. Specifically, we examined body condition as a predictor and the probability of breeding, number of offspring, and dispersal as outcomes of dominance. Additionally, we looked at variation in dominance between males and females and adults and yearlings, because marmots can engage in distinct interactions depending on the type of individuals involved. We found that marmots in better body condition have higher dominance rank than those in poorer condition. In addition, adults are dominant over yearlings. Within yearlings, dominance does not influence dispersal, but those in better body condition are less likely to disperse. Within all adults, individuals in better condition produce more offspring per year. Within adult males, more dominant males have greater reproductive success. Despite previous evidence of reproductive suppression in females, we found no effects of dominance rank on female reproductive success in the current study. The function of dominance in female marmots remains enigmatic.     

Longitudinal changes of dominance rank among the females of the Koshima group of Japanese monkeys

The changes of dominance rank among female Japanese monkeys of the Koshima group over a period of 29 years from 1957 were studied. The dominance rank order was relatively stable in the early population growing phase, while large scale-changes of dominance rank order occurred successively in the phase of population decrease brought about by the severe control of artificial feeding after 1972. Nevertheless, the rank order of several females of the highest status was stable. Furthermore, the reproductive success of these highest status females was high (Mori, 1979a;Watanabe et al., in prep.). Divergence of the dominance rank order fromKawamura's rules (Kawamura, 1958) was observed in the following respects: (1) Some females significantly elevated their rank depending on the leader males. (2) If mothers died when their daughters were still juveniles or nulliparous, the dominance rank of some of these offspring females was significantly lower than the mother's one. However 55% of daughters which lost their mothers at a young age inherited the mother's rank. (3) Dominance among sisters whose mother had died when at least one of the daughters was under 6 years old followed the rule of youngest ascendancy in 60% (Kawamura, 1958), and in 80% when both of the daughters were nulliparous at the mother's death. The mean rate of aggressive interactions for each female with subordinates to her was calculated by dividing the total aggressive interactions between the female in question and her subordinates by the number of subordinate females to the female in question. A female which showed a high rate of aggressive interactions with her subordinates was categorized as an “Attacker”, and a female showing a lower rate was categorized as a “Non-attacker”. Similarly, categories of “Attacked”, and “Non-attacked” were distinguished by using the rate of aggressive interactions with dominant females. Several females which were once categorized in one category in a year were repeatedly categorized in the same category over different years. The “Attacked” tended to be females of higher rank, and “Non-attackers” tended to be females of lower rank. “The second-higher-status females”, were “Attacked”, and their rank was unstable. In particular, females of lower rank within the lineage of the highest rank suffered this kind of severe status. Most of the daughters of these females showed a sharp drop of rank, and died when they were still at a young age, i.e. “the second-higher-status females” displayed low fitness. “Non-attackers” were significantly “Non-attacked”; i.e. they were females which showed a non-social attitude. Females which underwent a drop of rank tended to be “Non-attackers”. The most important factor which determined the females' rank was the memory of their dominance relations under the influence of their mother [dependent rank (Kawai, 1958)] in their early life during development. This finding corresponds well with the results in baboons obtained byWalter (1980); the target females of aggressive interactions by adolescent females were determined by the rank of the mothers when these adolescent females were born.     

Effects of maternal stress on egg characteristics in a cooperatively breeding fish

Elevated stress experienced by a mother can compromise both her own reproductive success and that of her offspring. In this study, we investigated whether chronically stressed mothers experienced such effects in cooperatively breeding species, in which helpers at the nest potentially compound the negative effects of maternal stress. Using Neolamprologus pulcher, a group-living cichlid fish from Lake Tanganyika, we observed the effects of experimentally increased stress on female reproductive success (measured as inter-spawn interval, and number of eggs) as well as egg characteristics including egg size and cortisol concentrations. Stress levels were manipulated by repeated exposure to the acute stresses of chasing and netting. Stressed females had longer inter-spawn intervals and laid fewer, smaller eggs. Although no significant differences in egg cortisol concentrations were detected between control and stressed females, egg cortisol concentration fell between spawns in control but not in stressed fish. No effect of helper number was detected for any parameter examined, except there appeared to be less change in egg cortisol content in groups with helpers present. Our results suggest that stress imposes fitness costs on breeding females, and social regulation of a dominance hierarchy does not appear to exacerbate or alleviate the negative effects of maternal stress.