Julie M. Worlein

Development in Japanese macaques (Macaca fuscata) : Sexually dimorphic behavior during the first year of life

We have documented several sexually dimorphic patterns of behavior that develop during the first year of life in infant Japanese macaques and their mothers. Mothers treated their infants differently by sex—mothers of males broke contact with them and retrieved them more frequently than did mothers of females. And mothers of male infants moved more frequently than did mothers of female infants. Male infants played more, played in larger groups, and mounted more frequently; female infants groomed and spent more time close to other monkeys in larger social groups than did males. Female infants were also punished by other group members more frequently than were male infants. We conclude that male and female Japanese macaque infants receive differential treatment early in life by both their own mothers and other animals, and males and females in turn treat their mothers and other animals differently. There appears to be a reciprocal relationship between the behavior of infants, mothers and other social partners that contributes to the development of sexually dimorphic patterns of behavior.

Development of partner preferences in Japanese Macaques (Macaca fuscata): Effects of gender and kinship during the second year of life

Quantitative data are presented on the effects of subject sex, partner sex,and kinship on the social interactions of 18 juveniles of the Oregon troop of Japanese macaques (Macaca fuscata).Data on these subjects as infants were also used to detail maturational changes in partner sex preferences. Nine males and nine females, whose multiparous mothers represented a cross section of dominance ranks, were observed using a focal-animal technique. Juveniles of both sexes engaged in more proximity, contact, grooming, mounting, aggression, and social play with kin than with nonkin partners. They initiated less contact with females and more contact with males during their second year. They initiated more grooming and aggression during their second year than their first year, with females displaying a strong preference for grooming females and males specifically aggressing males more during the second year. Aggression was higher between same-sexed partners than between opposite-sexed partners. Males engaged in more social interactions with males during the second year than the first year of life. Males played more than females during both years. Males played more with males during the second year than the first year, and males played with males more than did females during the second year. We conclude that sex differences in behavioral frequencies become evident during the first year of life, and sex differences in partner preferences emerge during the second year of life.

Social behavior of infant and mother Japanese Macaques (Macaca fuscata): Effects of kinship, partner sex, and infant sex

The behavioral interactions of 22 infant and mother Japanese macaques with other group members were studied. Focal-animal observations were made from the time of each infant’s birth until 1 year of age. Infants and mothers both displayed exceedingly strong preferences for associating with matrilineal kin and, specifically, for female kin. The degree of genetic relatedness was positively correlated with levels of spatial proximity, contact, grooming, aggression, and play. Overall frequencies of interactions with nonkin were very low, and partner sex was not an important factor in interactions with nonkin. There were no significant differences between male and female infants in interactions with kin versus nonkin. There was only one significant difference between male and female infants in interactions with males versus females: female infants showed stronger preferences for initiating proximity with females over males than did male infants. Because mothers provide the focal point for infant interactions during the first year of life, we compared the behavior of infants and mothers. Mothers were the recipients of more social interactions than were infants, mothers engaged in more grooming than did infants, and infants engaged in more social play than did mothers. These findings are only partially consistent with kin-selection theory, and the inadequacies of studying matrilineal kin discrimination to test kin selection are reviewed. The near-absence of infant sex differences in associations with social partners suggests that although maternal kin other than the mother are important to infant socialization, they probably do not contribute to the development of behavioral sex differences until after the first year of life.

Sex differences in Japanese macaques (Macaca fuscata): Effects of prenatal testosterone on juvenile social behavior

The aim of this study was to assess, in a nonhuman primate, the extent to which exposure to androgen during the prenatal period interacts with early social experience to affect the display of male or female patterns of behavior. Pregnant females from a large age-graded, heterosexual group of Japanese macaques (Macaca fuscata) were implanted about the 40th day of gestation with Silastic packets of testosterone. The packets were removed on the 100th day of gestation, and the females were allowed to give birth in their outdoor corral. An unplanned procedural change, by the surgeon who did the implants, created two groups of prenatally androgenized females: a high-dose group (N = 3), and a low-dose group (N = 4). The anatomical differentiation of these groups differed in that the high-dose group had small penises and no vaginas while the low-dose group had enlarged clitorises and patent vaginas. The behavior of these two groups of females was compared with that of normal males (N = 6), prenatally androgenized males (N = 6), and normal females (N = 5) from birth to 2 years of age. There were no differences between treated and normal males, but there were sex differences between males and normal females in the frequency of mounting, playing, displaying, and grooming. The high-dose group of prenatally androgenized females differed from normal females on only one measure: increased frequency of mounting. The low-dose group mounted other juveniles more frequently than did the normal females, but the difference was not statistically significant. We concluded that mounting behavior was most sensitive to the prenatal hormone environment because it showed the largest sex difference in normal animals. Given the small sample sizes, within-group variability could have obscured possible hormonal effects on other behaviors where sex differences were less dramatic.

Mating season effects on mother-infant conflict in Japanese macaques, Macaca fuscata

Abstract The impact of seasonal mating on the mother-infant relationship during the first year of the infants life was documented in a confined troop of Japanese macaques. During the weeks in which the mothers were being mounted, negative behaviour directed towards the infants increased. As maternal rejections and punishments escalated, the infants displayed regressive behaviour (showing signs of distress more frequently). Infants also groomed their mothers at an increased rate at this time. Behaviour that indicated increased independence did not show increases during this time. Moreover, behaviour negatively associated with independence, such as ventral contact and proximity to the mother, remained stable throughout this time period. The mother-infant relationship undergoes a period of conflict during the mating season not because the mother is weaning her infant, but because it is to her reproductive advantage to regulate the times in which the infant is allowed to suckle.

Alopecia in three macaque species housed in a laboratory environment

Alopecia is a persistent problem in captive macaque populations and despite recent interest, no factors have been identified that can unequivocally explain the presence of alopecia in a majority of cases. Seasonal, demographic, and environmental factors have been identified as affecting alopecia presentation in rhesus macaques, the most widely studied macaque species. However, few studies have investigated alopecia rates in other macaque species. We report alopecia scores over a period of 12 months for three macaque species (Macaca nemestrina, M. mulatta, and M. fascicularis) housed at three indoor facilities within the Washington National Primate Research Center (WaNPRC) in Seattle. Clear species differences emerged with cynomolgus (M. fascicularis) showing the lowest alopecia rates and pigtails (M. nemestrina) the highest rates. Further analysis of pigtail and rhesus (M. mulatta) macaques revealed that sex effects were apparent for rhesus but not pigtails. Age and seasonal effects were evident for both species. In contrast to previous reports, we found that older animals (over 10 years of age) had improved alopecia scores in comparison to younger adults. This is the first report on alopecia rates in pigtail macaques and the first comparison of alopecia scores in pigtail, cynomolgus, and rhesus macaques housed under similar conditions. Am. J. Primatol. 76:325–334, 2014.

Cognitive and motor deficits associated with HIV-2287 infection in infant pigtailed macaques: A nonhuman primate model of pediatric neuro-AIDS

Lentivirus-infected nonhuman primates exhibit behavioral and neurological pathology similar to human immunodeficiency virus (HIV)-infected humans and offer a means to examine the effects of lentivirus infection while controlling for confounding factors inherent in human populations. The purpose of this study was to examine cognitive and motor development in infant macaques vertically infected with HIV-2287. Subjects were 20 infant pigtail macaques (Macaca nemestrina); 8 controls born to uninfected dams, and 12 infants whose dams had been inoculated and infected with HIV-2287 in the third trimester of pregnancy. Eight of these pregnancies had undergone surgical procedures in the form of maternal amniotic catheters or maternal amniotic and fetal carotid artery and jugular vein catheters. Data indicated that catheterization had little or no impact on behavioral development. Seven infants were vertically infected (as measured by polymerase chain reaction (PCR) at birth) and five were not infected (as measured by PCR and coculture on repeated testing). Infected infants attained cognitive and motor milestones at significantly later ages than controls. Uninfected infants, born to infected dams, attained developmental milestones at later ages than controls on all tasks, but this reached statistical significance only for the Fine Motor Task. Attainment of milestones was not correlated with viral dose, maternal CD4+ levels at parturition or infant viral RNA levels at birth. Attainment of milestones was negatively correlated with infants’ proportions of CD4+ lymphocytes at birth and significantly correlated with proportions of CD4+ lymphocytes 2 weeks after birth, indicating poorer performance in those infants with a more rapid CD4+ depletion. These cognitive and motor deficits closely resemble those observed in human infants and children infected with HIV and indicate that HIV-2287-infected infant macaques represent an excellent model of pediatric neuro-acquired immunodeficiency syndrome (neuroAIDS).

Four decades of leading‐edge research in the reproductive and developmental sciences: The Infant Primate Research Laboratory at the University of Washington National Primate Research Center

The Infant Primate Research Laboratory (IPRL) was established in 1970 at the University of Washington as a visionary project of Dr. Gene (Jim) P. Sackett. Supported by a collaboration between the Washington National Primate Research Center and the Center on Human Development and Disability, the IPRL operates under the principle that learning more about the causes of abnormal development in macaque monkeys will provide important insights into the origins and treatment of childhood neurodevelopmental disabilities. Over the past 40 years, a broad range of research projects have been conducted at the IPRL. Some have described the expression of normative behaviors in nursery‐reared macaques while others have focused on important biomedical themes in child health and development. This article details the unique scientific history of the IPRL and the contributions produced by research conducted in the laboratory. Past and present investigations have explored the topics of early rearing effects, low‐birth‐weight, prematurity, birth injury, epilepsy, prenatal neurotoxicant exposure, viral infection (pediatric HIV), diarrheal disease, vaccine safety, and assisted reproductive technologies. Data from these studies have helped advance our understanding of both risk and resiliency in primate development. New directions of research at the IPRL include the production of transgenic primate models using our embryonic stem cell‐based technology to better understand and treat heritable forms of human intellectual disabilities such as fragile X. Am. J. Primatol. 75:1063–1083, 2013.

Responses to the Human Intruder Test are related to hair cortisol phenotype and sex in rhesus macaques (Macaca mulatta)

Measurement of cortisol in hair provides a chronic index of hypothalamic–pituitary–adrenal (HPA) axis activity and has been applied to assessments of temperament (stable behavioral differences between individuals). However, the extent to which chronically high HPA axis activity relates to a correspondingly high degree of behavioral reactivity is as yet unknown. Therefore, the goal of the present experiment was to assess the relationship between hair cortisol and a reactive temperament. We administered the Human Intruder Test (HIT) twice to 145 (80 male) rhesus macaques (Macaca mulatta) in order to assess behavioral reactivity. The HIT presents monkeys with an unfamiliar experimenter and is composed of a Baseline phase (no intruder) followed by three experimental phases in which the orientation of the intruder changes (Profile, Stare, Back). Behavioral responses to the test were videotaped and behaviors thought to reflect a reactive response to the intruder were scored for duration. Hair samples collected within ±1 month of the first HIT session were analyzed for cortisol by enzyme immunoassay. Subjects were assigned to three groups based on hair cortisol concentration: high, intermediate, and low cortisol phenotypes. Monkeys with the high cortisol phenotype were more reactive to the presence of the intruder than those with the low cortisol phenotype: they were more aggressive, scratched more, and spent more time in the back half of the cage. Males yawned significantly more while females spent more time immobile and in the back of the cage. Overall, monkeys with higher hair cortisol demonstrated an exaggerated response to the presence of the human intruder, supporting a relationship between high levels of chronic HPA axis activity and a reactive temperament. These results indicate that high levels of HPA axis activity, which may result from either genetic variation or environmental stress, correspond with heightened behavioral responses to a stressful experience. Am. J. Primatol. 79:e22526, 2017.

Assessing significant (>30%) alopecia as a possible biomarker for stress in captive rhesus monkeys (Macaca mulatta)

Hair loss is common in macaque colonies. Very little is known about the relationship between psychological stress and hair loss. We initially examined alopecia and hair cortisol concentrations in 198 (89 male) rhesus macaques from three primate centers and demonstrated replicability of our previous finding that extensive alopecia (>30% hair loss) is associated with increased chronic cortisol concentrations and significantly affected by facility. A subset of these monkeys (142 of which 67 were males) were sampled twice approximately 8 months apart allowing us to examine the hypotheses that gaining hair should be associated with decreases in cortisol concentrations and vice versa. Hair loss was digitally scored using ImageJ software for the first sample. Then visual assessment was used to examine the second sample, resulting in three categories of coat condition: (i) monkeys that remained fully haired; (ii) monkeys that remained alopecic (with more than 30% hair loss); or (iii) monkeys that showed more than a 15% increase in hair. The sample size for the group that lost hair was too small to be analyzed. Consistent with our hypothesis, monkeys that gained hair showed a significant reduction in hair cortisol concentrations but this effect only held for females. Coat condition changed little across sampling periods with only 25 (11 male) monkeys showing a greater than 15% gain of hair. Twenty (7 male) monkeys remained alopecic, whereas 97 (49 males) remained fully haired. Hair cortisol was highly correlated across samples for the monkeys that retained their status (remained alopecic or retained their hair). Am. J. Primatol. 79:e22547, 2017.