Sex and age differences in juvenile social priorities in female philopatric,nondespotic blue monkeys

Juveniles should choose social partners on the basis of both current and future utility. Where one sex is philopatric, one expects members of that sex to develop greater and sex‐typical social integration with group‐mates over the juvenile period. Where a partner's position in a dominance hierarchy is not associated with services it can provide, one would not expect juveniles to choose partners based on rank, nor sex differences in rank‐based preferences. We tested these ideas on 39 wild juvenile (3.2–7.4 years) blue monkeys (Cercopithecus mitis stuhlmanni), cercopithecines with strict female philopatry and muted hierarchies. We made focal animal observations over 6 months, and computed observed:expected amounts of proximity time, approaches and grooming given to various social partners. Overall, our results agree with the hypothesis that juvenile blue monkeys target social partners strategically. Spatial proximity, approaches and active grooming showed similar patterns regarding juvenile social preferences. Females were far more sociable than males, groomed more partners, reciprocated grooming more frequently, and preferred—while males avoided—infants as partners. Older juveniles (5–7 years) spent more time than younger juveniles (3–4 years) near others, and older females were especially attracted to infants. Close kin, especially mothers and less consistently adult sisters, were attractive to both male and female juveniles, regardless of age. Both sexes also preferred same‐sex juveniles as social partners while avoiding opposite‐sex peers. Juveniles of both sexes and ages generally neither preferred nor avoided nonmaternal adult females, but all juveniles avoided adult males. Partner's rank had no consistent effect on juveniles' preference, as expected for a species in which dominance plays a weak role. Juveniles' social preferences likely reflect both future and current benefits, including having tolerant adult kin to protect them against predators and conspecifics, same‐sex play partners, and, for females, infants on which to practice mothering skills. Am. J. Primatol. 72:193–205, 2010. © 2009 Wiley‐Liss, Inc.     

Maternal effect genes and the evolution of sociality in haplo-diploid organisms

Maternal care and female-biased sex ratios are considered by many to be essential prerequisites for the evolution of eusocial behaviors among the hymenoptera. Using population genetic models, I investigate the evolution of genes that have positive maternal effects but negative, direct effects on offspring fitness. I find that, under many conditions, such genes evolve more easily in haplo-diploids than in diplo-diploids. In fact, the conditions are less restrictive than those of kin selection theory, which postulate genes with negative direct effects but positive sib-social effects. For example, the conditions permitting the evolution of maternal effect genes are not affected if females mate multiply, whereas multiple mating reduces the efficacy of kin selection by reducing genetic relatedness within colonies. Inbreeding also differentially facilitates evolution of maternal effect genes in haplo-diploids relative to diplo-diploids, although it does not differentially affect the evolution of sib-altruism genes. Furthermore, when the direct, deleterious pleiotropic effect is restricted to sons, a maternal effect gene can evolve when the beneficial maternal effect is less than half (with inbreeding, much less) of the deleterious effect on sons. For kin selection, however, the sib-social benefits must always exceed the direct costs because genetic relatedness is always less than or equal to 1.0. The results suggest that haplo-diploidy facilitates (1) the evolution of maternal care, and (2) the evolution of maternal effect genes with antagonistic pleiotropic effects on sons. The latter effect may help explain the tendency toward female-biased sex ratios in haplo-diploids, especially those with inbreeding. I conclude that haplo-diploidy not only facilitates the evolution of sister-sister altruism by kin selection but also facilitates the evolution of maternal care and female-biased sex ratios, two prerequisites for eusociality.     

The ontogeny of sex differences in the behavior of patas monkeys

Many studies of sex differences in primates have been based on small experimental groups of peers in which only a limited range of social behavior could be expressed. In addition, the first few months of life are often the focus of such studies, with relatively little attention paid to older juveniles. In this study, 11 male and 9 female juvenile patas monkeys, living in a captive social group with all age-sex classes available, were observed between 1 and 4 years of age. A subset of seven patas monkeys was also observed between birth and 1 year of age. Here, we report the development of sex differences in independence, play, grooming, positioning behavior, and aggression over the juvenile period. Juvenile male patas monkeys played more and in longer bouts than females, but wrestling (rough-and-tumble play) was not more common among males. There were few differences in behaviors directed to male and female juveniles by other group members. Distinct differences emerged only in the behaviors of the juveniles themselves, with females being more active participants in social and aggressive interactions than males. In general, sex differences in patas monkeys show a mixture of patterns, some of which are predictive of adult sex differences and some of which appear to be specific to the particular demands of the juvenile period in this species     

Behavior and endocrine concentrations do not distinguish sex in monomorphic juvenile howlers (Alouatta palliata)

Behavioral observations on juvenile mantled howlers are limited by visually undifferentiated genitalia; however, animals can be sexed when they are very young or if they are captured. Behavioral data and fecal samples from juveniles during month-long field studies from 1993 to 1995 were analyzed to determine whether there are developmental differences in behavior or hormone concentrations that can be used to differentiate males from females. The subjects were juveniles of known sex and age from five different social groups on Hacienda La Pacifica, Costa Rica. Based on 749.8 hr of focal-animal sampling, there were no sex differences in daily activity patterns. There were no sex differences in proximity to mothers and other group members, and age differences reflected howler life-history patterns. There were no differences in estradiol or testosterone concentration by age or sex. Juvenile monomorphy thus extends beyond morphology to behavioral and hormonal similarity as well. Most juveniles are forced out of their natal groups and remain solitary until they join new groups by supplanting all same-sex adult group members. Monomorphy may allow them to spend more time in natal groups, and thus both reduce the solitary period and allow the juveniles to improve social skills needed for later immigration. While this strategy may benefit juvenile howlers, it remains a problem for those who wish to study juvenile sex differences from a distance.     

Sex differences in the social behavior of wild spider monkeys (Ateles geoffroyi yucatanensis)

Competition for resources and the need for cooperation are reported to affect patterns of social interactions and thus the quality of social relationships in primates. Relationships may be described as high quality when both individuals behave in a way that benefits their partner. We investigated the distribution of a wide range of social behaviors across sex partner combinations of adult spider monkeys with specific reference to contested resources. Data were collected from two communities of wild spider monkeys (Ateles geoffroyi yucatanensis) in the Otoch Ma'ax Yetel Kooh reserve in Yucatan, Mexico. Affiliative behavior was exchanged most frequently between males, and as male-male aggression was rare, male-male social relationships were characterized as high quality. Female-female social relationships were best described as low quality as females showed no preference to be in proximity with other females and female-female affiliative behavior was rare. Relationships between the sexes generally were characterized by high rates of female-directed male aggression, although additional investigation into the effects of kinship and female reproductive state on male-female relationships is required before further conclusions can be drawn. Dyadic and coalitionary female-female aggression was significantly higher than expected in a feeding context, confirming that female spider monkeys primarily compete for access to food. Male-male aggression did not increase significantly when in the presence of females, but males embraced at higher rates when in mixed-sex subgroups. As embraces serve to reduce the likelihood of aggression during tense situations, high rates of male-male embraces in mixed-sex subgroups may mitigate male conflicts over access to females.     

Conditions of failure and recovery of maternal behavior in captive squirrel monkeys (Saimiri)

This paper deals with the functioning and malfunctioning of maternal behavior in relation to external and social conditions. During developmental studies in captive squirrel monkey groups, 49 mother-infant pairs were observed. There were several cases of maternal inadequacy subsequent to (1) postnatal transportation, (2) exaggerated social investigation by immatures,and (3) premature allomothering. Brief mother-infant separations by humans did not yield such failures. One female consistently prevented nursing with at least three of her five viable offspring. Complete or partial failure of maternal behavior did not preclude subsequent recovery and/or adequate allomothering. Dedicated to Prof. Dr. Med. Detlev Ploog on the occasion of his 60th birthday.     

Sex differences in juvenile mouse social behavior are influenced by sex chromosomes and social context

Play behavior in juvenile primates, rats and other species is sexually dimorphic, with males showing more play than females. In mice, sex differences in juvenile play have only been examined in out-bred CD-1 mice. In this strain, contrary to other animals, male mice display less play soliciting than females. Using an established same-sex dyadic interaction test, we examined play in in-bred C57BL/6J (B6) 21-day-old mice. When paired with non-siblings, males tended to be more social than females, spending more time exploring the test cage. Females displayed significantly more anogenital sniffing and solicited play more frequently than did males. To determine if the origin of the sex difference was sex chromosome genes or gonadal sex, next we used the four core genotype mouse. We found significant interactions between gonadal sex and genotype for several behaviors. Finally, we asked if sibling pairs (as compared to non-siblings) would display qualitatively or quantitatively different behavior. In fact, XX females paired with a sibling were more social and less exploratory or investigative, whereas XY males exhibited less investigative and play soliciting behaviors in tests with siblings. Many neurobehavioral disorders, like autism spectrum disorder (ASD), are sexually dimorphic in incidence and patients interact less than normal with other children. Our results suggest that sex chromosome genes interact with gonadal hormones to shape the development of juvenile social behavior, and that social context can drastically alter sex differences. These data may have relevance for understanding the etiology of sexually dimorphic disorders such as ASD.     

Sexually dimorphic transitions revealed in the relationships of yearling rhesus monkeys following the birth of siblings

We report here that in a large captive group of monkeys, Macaca mulatta,sudden sex-related changes occur in social interactions in one short phase of an infant’s development. Social interactions of 1-year-old animals (males, N =12; females, N =8) 6 weeks before the birth of siblings were compared with interactions occurring 6 weeks after the birth. On the day of the siblings’ birth, depression-like postures were seen in two yearling males (YMs); 10 YMs showed hyperactivity. In the postbirth period, YMs refocused their attentions away from their mother and toward other, often unrelated members of the group. Although YMs initiated disengagement of interactions with their mothers, there was evidence that mothers attempted to lessen this disengagement. The YMs had close relationships with specific (“preferred”) male individuals. These relationships (particularly those with adult males) became more pronounced following the birth of the sibling. The adult-male group also took an active role in maintaining interactions with YMs. The preferred partners in the YM-other male relationship before the birth of the sibling were, however, not always the same as those in the period after the birth. Dominance relationships and probably genetic factors determined patterns of interaction between YMs and their preferred male partners. Among yearling females (YFs), no dramatic changes in interactions with their mothers or with other group members were detected after their mothers gave birth. Relationships in YF-mother and YF-other-individual pairs (especially when the other individual was kin) seemed to be consolidated during the postbirth interval. There was little evidence of jealousy between the YFs and their younger siblings. Thus, sibling birth acted as a stimulus for the occurrence of sexually dimorphic interactions in yearlings. We suggest that in natural environments, social interactions in YFs promote relationships that will serve to integrate them into the matrilineal social structure, whereas comparable behavior in YMs encourages relationships with males that they may emigrate with into, or meet again in, nonnatal troops.     

Early environment influences later performance in fishes

Conditions fish encounter during embryogenesis and early life history can leave lasting effects not only on morphology, but also on growth rate, life‐history and behavioural traits. The ecology of offspring can be affected by conditions experienced by their parents and mother in particular. This review summarizes such early impacts and their ecological influences for a variety of teleost species, but with special reference to salmonids. Growth and adult body size, sex ratio, egg size, lifespan and tendency to migrate can all be affected by early influences. Mechanisms behind such phenotypically plastic impacts are not well known, but epigenetic change appears to be one central mechanism. The thermal regime during development and incubation is particularly important, but also early food consumption and intraspecific density can all be responsible for later life‐history variation. For behavioural traits, early experiences with effects on brain, sensory development and cognition appear essential. This may also influence boldness and other social behaviours such as mate choice. At the end of the review, several issues and questions for future studies are given.     

Maternal protectiveness and response to the unfamiliar in vervet monkeys

Vervet monkeys (Cercopithecus aethiops sabaeus) show individual differences in approach-avoidance behavior when faced with an unfamiliar and potentially threatening situation. Prior research from our colony demonstrated that juveniles who had experienced high levels of early maternal protectiveness were more cautious in response to novelty, compared to juveniles who had had less protective mothers. The research reported here was designed to verify this result in a paradigm that experimentally varied maternal protectiveness through the introduction of new breeding adult males. Mothers responded to the presence of new males by increased maternal protectiveness toward infants born in the year following the introductions. Individual differences in response to the unfamiliar were later evaluated by measuring the latency to approach within 1 m of novel food containers placed into the home enclosure of four naturally composed social groups. Infants approached with the same latency and in the same order as their mothers. Juveniles approached sooner than, and independent of, their mother's current behavior, but their latency to approach could be predicted by the experimentally induced variation in maternal protectiveness they had experienced as infants. Immatures who had been born in New Male years, when maternal protectiveness was high, were more cautious and had significantly longer latencies to approach the novel stimulus compared to immatures who had been born in Resident Male years. © 1993 Wiley-Liss, Inc.     

Species differences in the interest shown in infants by juvenile female macaques (Macaca radiata andM. mulatta)

Using a focal animal technique, 16 juvenile female rhesus and bonnet macaques (2–3 years old) were observed with respect to the frequency and duration of their contacts with infants (0–1 year old). Each of these subjects was a member of one of four seminatural groups of macaques housed in 0.5-acre field cages at the California Primate Research Center. Rhesus juvenile females became very interested in infants when the latter were quite young, and maintained that interest throughout the study. When the infants were approximately 3–4 months old, the rhesus juveniles spent, on the average, 3.9 min/hr with those infants. By the time the infants were yearlings, the time spent with infants was approximately 6 min/hr. Relative to the rhesus, the bonnet juveniles showed less interest (about 2.2 min/hr) in young (3- to 4- month-old) infants, although by the time the infants were yearlings, the bonnets spent about 5.6 min/hr with them. Rhesus juveniles preferred sibling over nonsibling infants, but the presence of a sibling was not a necessary requirement for infant-directed behavior. The two bonnet juveniles who had infant siblings showed no preference for the latter. These data were interpreted within the framework of Quiatt’s [(1979) Am. Anthropol. 81: 310–319 conclusions about allomaternal behavior. Specifically, it was argued that, to the extent that there are species differences in maternal behavior, there should also be species differences in allomaternal behavior. The species differences in the maternal styles of rhesus and bonnet macaques provide a basis for an examination of this hypothesis.     

Old,socially housed rhesus monkeys manipulate objects

Recent research has indicated that old, individually housed monkeys show little interest in novel objects. Yet unanswered is whether this effect is caused primarily by age or housing condition. The purpose of this study was to assess the role of social living in promoting responsiveness to objects. We measured the rates of object manipulation in older animals, assessed responsiveness over time to particular objects as a measure of habituation, and examined social influences on object use. Several social groups of rhesus monkeys that contained older adults were studied. These groups were housed in indoor pens or in an outdoor enclosure, and all monkeys had continuous access to a variety of objects in their home environment. In contrast to previous studies of individually housed monkeys, our group-housed monkeys showed sustained interest in objects. Old monkeys manipulated objects extensively, and this response was all the more significant, given that the objects were not novel. Monkeys housed in an outdoor enclosure showed object manipulation patterns that were not different from monkeys housed in indoor pens. However, females exhibited much higher object-related responses than males. Social facilitation played a role in the reactions of some monkeys to objects. Patterns of social facilitation as well as avoidance were present in two of the three indoor groups that were observed. Failure to manipulate objects in rhesus macaques appears to be more a function of individual housing than of old age. Factors such as environmental complexity, social needs, and early experience should be considered in order to understand why individually housed rhesus monkeys are unresponsive to objects. © 1993 Wiley-Liss, Inc.     

Among-sibling differences in the phenotypes of juvenile fish depend on their location within the egg mass and maternal dominance rank

We investigated whether among-sibling differences in the phenotypes of juvenile fish were systematically related to the position in the egg mass where each individual developed during oogenesis. We sampled eggs from the front, middle and rear thirds of the egg mass in female brown trout of known dominance rank. In the resulting juveniles, we then measured traits that are related to individual fitness: body size, social status and standard metabolic rate (SMR). When controlling for differences among females in mean egg size, siblings from dominant mothers were initially larger (and had a lower mass-corrected SMR) if they developed from eggs at the rear of the egg mass. However, heterogeneity in the size of siblings from different positions in the egg mass diminished in lower-ranking females. Location of the egg within the egg mass also affected the social dominance of the resulting juvenile fish, although the direction of this effect varied with developmental age. This study provides the first evidence of a systematic basis for among-sibling differences in the phenotypes of offspring in a highly fecund organism.     

Juvenile hormone in earwigs: Roles in oogenesis,mating, and maternal behaviors

The role of juvenile hormone (JH) in courtship, mating, maternal behavior, and the ovarian cycle was studied in the ring-legged earwig, Euborellia annulipes (Lucas). The single, median corpus allatum makes and secretes JH III. JH III production was low in newly eclosed adult females, increasing as oocytes developed, maximal at about the time of oviposition, and low again in brooding females. Application of 35 or 122 μg JH III to newly eclosed females hastened the onset of courtship behavior, but had no effect on the age at which females first mated nor on the duration of mating, though the trend is toward advanced onset. Hormone treatment advanced the age of first oviposition and reduced clutch size and the proportion of eggs hatching but did not affect the interval from oviposition of the first clutch to oviposition of the second clutch, nor the size and proportion hatching of the second clutch. Acetone treatment and treatment with 6 μg JH III did not affect these parameters. Application of 50 μg JH III to females on the day of oviposition shortened the duration of maternal care and advanced the onset of the second gonadotropic cycle, compared with that of acetone-treated and precocene II-treated females. The duration of maternal care was positively correlated with the proportion of eggs hatching. JH titer analysis confirmed JH III to be the predominant hormone in this species and clearly demonstrated the absence of other homologues. This work also confirmed our hypothesis that intermediate to high levels of JH are associated with oocyte growth, mating, and cessation of maternal care; low levels of JH are associated with the period of maternal behavior and slow ovarian development. We are currently investigating factors which might regulate corpus allatum activity during the reproductive cycle and the subsequent period of maternal care. Arch. Insect Biochem. Physiol. 35:427–442, 1997. © 1997 Wiley-Liss, Inc.     

High‐fiber diet promotes weight loss and affects maternal behavior in vervet monkeys

The dramatic increase in obesity in western societies has shifted the emphasis in nutrition research from the problems of undernutrition to the adverse consequences of being overweight. As with humans, Old World monkeys are at increased risk for type II diabetes and other chronic diseases when they gain excessive weight. To prevent overweight and obesity, promote animal health, and provide a more natural level of fiber in the diet, the standard commercial monkey chow diet at a vervet monkey breeding colony was changed to a higher fiber formulation in 2004. The new diet was also higher in protein and lower in carbohydrate and energy density than the standard diet. Because maternal behavior is known to be sensitive to differences in resource availability, data on weight and mother–infant interactions for 147 mothers with 279 infants born from 2000 through 2006 were assessed for effects of the diet change. The results showed that, even though food was provided ad libitum, the mean body weight of breeding females was 10% lower after the transition to the high‐fiber diet. Behaviorally, mothers on the high‐fiber diet were significantly more rejecting to their infants, and their infants had to play a greater role in maintaining ventral contact in the first few months of their lives. The effects of the diet change on maternal rejection were significantly related to the mother's body weight, with lower‐weight mothers scoring higher in maternal rejection. These results demonstrate that maternal behavior is responsive to changes in maternal condition, and that beneficial changes in the diet may have unintended consequences on behavior. Am. J. Primatol. 72:234–241, 2010. © 2009 Wiley‐Liss, Inc.     

Sex-specific sibling interactions and offspring fitness in vertebrates: patterns and implications for maternal sex ratios

Vertebrate sex ratios are notorious for their lack of fit to theoretical models, both with respect to the direction and the magnitude of the sex ratio adjustment. The reasons for this are likely to be linked to simplifying assumptions regarding vertebrate life histories. More specifically, if the sex ratio adjustment itself influences offspring fitness, due to sex-specific interactions among offspring, this could affect optimal sex ratios. A review of the literature suggests that sex-specific sibling interactions in vertebrates result from three major causes: (i) sex asymmetries in competitive ability, for example due to sexual dimorphism, (ii) sex-specific cooperation or helping, and (iii) sex asymmetries in non-competitive interactions, for example steroid leakage between fetuses. Incorporating sex-specific sibling interactions into a sex ratio model shows that they will affect maternal sex ratio strategies and, under some conditions, can repress other selection pressures for sex ratio adjustment. Furthermore, sex-specific interactions could also explain patterns of within-brood sex ratio (e.g. in relation to laying order). Failure to take sex-specific sibling interactions into account could partly explain the lack of sex ratio adjustment in accordance with theoretical expectations in vertebrates, and differences among taxa in sex-specific sibling interactions generate predictions for comparative and experimental studies.     

Context-dependent sex allocation: constraints on the expression and evolution of maternal effects

Despite decades of research, whether vertebrates can and do adaptively adjust the sex ratio of their offspring is still highly debated. However, this may have resulted from the failure of empirical tests to identify large and predictable fitness returns to females from strategic adjustment. Here, we test the effect of diet quality and maternal condition on facultative sex ratio adjustment in the color polymorphic Gouldian finch (Erythrura gouldiae), a species that exhibits extreme maternal allocation in response to severe and predictable (genetically-determined) fitness costs. On high-quality diets, females produced a relatively equal sex ratio, but over-produced sons in poor dietary conditions. Despite the lack of sexual size dimorphism, nutritionally stressed foster sons were healthier, grew faster, and were more likely to survive than daughters. Although these findings are in line with predictions from sex allocation theory, the extent of adjustment is considerably lower than previously reported for this species. Females therefore have strong facultative control over sex allocation, but the extent of adjustment is likely determined by the relative magnitude of fitness gains and the ability to reliably predict sex-specific benefits from environmental (vs. genetic) variables. These findings may help explain the often inconsistent, weak, or inconclusive empirical evidence for adaptive sex ratio adjustment in vertebrates.     

Correlates of sexual and maternal competence in captive gorillas

The captive gorilla population may not be self-sustaining, in part because the overall birth rate is low and because many potential founders have failed to reproduce. We used questionnaires to collect standardized biographies of every gorilla held in North America. These biographies were searched for factors associated with reproductive success or failure. Captive-born gorillas are reproducing at least as well as wild-borns, when reproductive success is expressed as number of infants per year of reproductive opportunity. Mother-reared females are reproductively more successful than hand-reared females, but there is no difference in the reproductive success of mother-reared and hand-reared males. Social access to conspecifics in the 1st year is associated with higher reproductive success, at least for females. Reproductively successful and unsuccessful gorillas of both sexes have had equal access to potential mates, but unsuccessful animals are less likely than successful ones to exhibit normal sexual behavior. We conclude that many cases of reproductive failure are due to deficits in sexual behavior, which in turn may result from lack of early social experience with conspecifics. Some reproductive failure involves medical problems; interventive diagnostic techniques continue to be useful, if only to identify healthy individuals that can be managed intensively. The probability that a female will be a competent mother is not affected by her being wild-born or captive-born, or mother-reared or hand-reared.     

Genetic architecture and maternal contributions of early‐life survival in lake trout Salvelinus namaycush

The influences of additive, non‐additive and maternal effects on early survival (uneyed embryo survival, eyed embryo survival, alevin survival and overall survival to first feeding) were quantified in lake trout Salvelinus namaycush using a 7 × 7 full‐factorial breeding design. Maternal effects followed by non‐additive genetic effects explained around one third of the phenotypic variance of the survival traits. Although the amount of additive genetic effects were low (<1%), suggesting a limited potential of the traits to respond to new selection pressures, how maternal and non‐additive genetic effects may respond to selection under certain circumstances are discussed.