Behavioral Inhibition in Rhesus Monkeys (Macaca mulatta) Is Related to the Airways Response, but Not Immune Measures, Commonly Associated with Asthma

Developmental Psychobiology

2018

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The effects of early stress may not be limited to the exposed generation, but are sometimes passed on to subsequent generations. Such non-genetic transgenerational inheritance is a potentially important developmental and evolutionary force. We compared the transgenerational effects of maternal and paternal line early stress on anxiety- and health-related traits in three non-exposed generations (F1, F2 and F3) of semi-naturalistically raised rhesus macaques. As infants, F0 macaques were exposed to nursery rearing (NR) or semi-naturalistic social conditions (CONTROL). Three hundred forty non-exposed F1-F3 descendants were CONTROL reared and physiological and behavioral measures were collected during standardized assessment at 3-4 months of age. Paternal line NR was significantly associated with greater nervousness in F1-F3 and lower immune cell counts in F1-F2. Maternal-line NR effects were not observed. This study suggests that acquired stress-related traits may be "inherited" across generations in primates, through complex social or germ-line mechanisms.

Section: Discussionmentioning

confidence: 99%

Paternal line effects of early experiences persist across three generations in rhesus macaques

Kinnally

Gonzalez

Developmental Psychobiology

2018

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“…For juvenile assessments (relocation cage observation and human intruder challenge), animals were relocated from their outdoor field corrals and placed in an individual holding cage (same construction and dimensions as during the infant assessments) for a total of four days, and then returned to the outdoor field corral. Behavioral testing for Day 1 is presented here, while data collected during Days 2, 3, and 4 are presented elsewhere (Chun et al, 2013). Juveniles were provided with a Nylabone Dental Chew (Nylabone, Neptune, NJ), a mirror, water ad libitum, and monkey chow twice daily between 0700 h and 0900 h and between 1400 h and 1500 h.…”

Section: Subjects and Living Arrangementsmentioning

confidence: 99%

“…The relationship between BI and levels of cortisol is unclear in previous studies, however; BI has been linked to a blunted cortisol reactivity (Gunnar, Wewerka, Frenn, Long & Griggs, ), high baseline levels (Kagan et al ., ; Schmidt et al ., ), or no reactivity changes (de Haan, Gunnar, Tout, Hart & Stansbury, ) in humans. Although there are mixed results for cortisol values in the literature, the current study utilized the same criteria described in our two previous studies (Capitanio et al ., ; Chun et al ., ), which, in combination, did show predictive validity for an important health‐related outcome.…”

Section: Introductionmentioning

confidence: 97%

“…Previous work in our lab has characterized BI in infant rhesus monkeys to understand the association of BI and negative health outcomes (Capitanio, Miller, Schelegle, Mendoza, Mason et al, 2011;Chun, Miller, Schelegle, Hyde & Capitanio, 2013). When infants were 3-4 months old, they were relocated and separated from their mother for a 25-hour period (see BioBehavioral Assessment Program below).…”

Section: Introductionmentioning

confidence: 99%

“…When infants were 3-4 months old, they were relocated and separated from their mother for a 25-hour period (see BioBehavioral Assessment Program below). The criteria used to characterize BI included: (a) low Emotionality during the behavioral observations conducted in the first hour following relocation consisting of decreased rate of vocalizations, threats, lipsmacks, and scratching; (b) high Vigilance from temperament ratings conducted at the end of the 25-hour period, which was a composite of: vigilant, not depressed, not tense, and not timid; and (c) a blunted cortisol response 7 hours after relocation/separation (Capitanio et al, 2011;Chun et al, 2013). Low emotionality (Kalin & Shelton, 1989Rogers et al, 2008) and high vigilance (Fox, Henderson, Marshall, Nichols & Ghera, 2005;Kagan et al, 1987) are characteristics that are similar to those used to describe behaviorally inhibited monkeys and children in previous studies.…”

Section: Introductionmentioning

confidence: 99%

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Developmental consequences of behavioral inhibition: a model in rhesus monkeys (Macaca mulatta)

Chun

2015

Developmental Science

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In children, behavioral inhibition is characterized by a disposition to withdraw in the presence of strangers and novel situations. Later in life, behavioral inhibition can result in an increased risk for anxiety and depression and a decrease in social behavior. We selected rhesus monkeys that, during infancy, showed evidence of behavioral inhibition in response to separation, and contrasted them with non-inhibited peers. To understand the development of behavioral inhibition at juvenile age, we collected behavioral data in response to relocation; in response to a human intruder challenge; and in naturalistic outdoor field corrals. At four years of age (young adulthood), we again collected behavioral data in the outdoor field corrals to understand the adult social consequences of behavioral inhibition. We also included sex, dominance rank, and number of available kin in our analyses. Finally, to understand the consistency in behavior in behaviorally inhibited animals, we conducted exploratory analyses contrasting behaviorally inhibited animals that showed high vs. low durations of non-social behaviors as adults. At juvenile age, behaviorally inhibited animals continued to show behavioral differences in the novel testing room and during the human intruder challenge, generally showing evidence of greater anxiety and emotionality compared to non-inhibited controls. In their outdoor corrals, behaviorally inhibited juveniles spent more time alone and less time in proximity and grooming with mother and other adult females. In young adulthood, we found that behavioral inhibition was not related to time spent alone. We did find that duration of time alone in adulthood was related to time alone exhibited as juveniles; sex, dominance rank, or the number of kin were not influential in adult non-social duration, either as main effects or as moderators. Finally, exploratory analyses revealed that behaviorally inhibited females that were more sociable (less time spent alone) as adults had spent more time grooming as juveniles, suggesting that high quality social interaction at a young age might mitigate the social consequences of behavioral inhibition. Overall, we believe that the many similarities with the human data that we found suggests that this monkey model of naturally occurring behavioral inhibition can be valuable for understanding social development.

The relationship of maternal rank, 5‐HTTLPR genotype, and MAOA‐LPR genotype to temperament in infant rhesus monkeys (Macaca mulatta)

Sommet

Rosso

2022

American J Primatol

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Temperament is a construct whose manifestations are quantifiable from an early age, and whose origins have been proposed as "biological." Our goal was to determine whether maternal rank and infant genotype are associated with five measures of temperament in 3-to 4-month old rhesus monkeys (Macaca mulatta), all of whom were born and reared by their mothers in large, outdoor, half-acre cages.Maternal rank was defined as the proportion of animals outranked by each female, and the two genes of interest to us were monoamine oxidase and serotonin transporter, both of which are polymorphic in their promoter regions (MAOA-LPR and 5-HTTLPR, respectively), with one allele of each gene considered a "plasticity" allele, conferring increased sensitivity to environmental events. Our large sample size (n = 2014-3140) enabled us to examine the effects of individual genotypes rather than combining genotypes as is often done. Rank was positively associated with Confident temperament, but only for animals with the 5-repeat allele for MAOA-LPR. Rank had no other effect on temperament. In contrast, genotype had many different effects, with 5-HTTLPR associated with behavioral inhibition, and MAOA-LPR associated with ratings-based measures of temperament. We also examined the joint effect of the two genotypes and found some evidence for a doseresponse: animals with the plasticity alleles for both genes were more likely to be behaviorally inhibited. Our results suggest phenotypic differences between animals possessing alleles for MAOA-LPR that show functional equivalence based on in vitro tests, and our data for 5-HTTLPR revealed differences between short/short homozygotes and long/short heterozygotes, strongly suggesting that combining genotypes for statistical analysis should be avoided if possible. Our analysis also provides evidence of sex differences in temperament, and, to our knowledge, the