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Paternal Early Experiences Influence Infant Development Through Non-social Mechanisms in Rhesus Macaques

Overview
Journal Front Zool
Publisher Biomed Central
Specialty Biology
Date 2016 Jan 28
PMID 26816514
Citations 16
Authors
Affiliations
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Abstract

Background: Early experiences influence the developing organism, with lifelong and potentially adaptive consequences. It has recently become clear that the effects of early experiences are not limited to the exposed generation, but can influence physiological and behavioral traits in the next generation. Mechanisms of transgenerational effects of parental early experiences on offspring development are often attributed to prenatal or postnatal parental influence, but recent data suggest that germ-line plasticity may also play a role in the transgenerational effects of early experiences. These non-genetic transgenerational effects are a potentially important developmental and evolutionary force, but the effects of parental experiences on behavior and physiology are not well understood in socially complex primates. In the non-human primate, the rhesus macaque, nursery rearing (NR) is an early life manipulation used for colony management purposes, and involves separating infants from parents early in life. We examined the effects of maternal and paternal early NR on infant rhesus macaque immunity, physiology, and behavior.

Results: We theorized that differences in behavior or physiology in the absence of parent-offspring social contact would point to biological and perhaps germ-line, rather than social, mechanisms of effect. Thus, all subjects were themselves NR. Male and female infant rhesus macaques (N= 206) were separated from parents and social groups in the first four days of life to undergo NR. These infants differed only in their degree of NR ancestry - whether their dams or sires were themselves NR. At 3-4 months of age, infants underwent a standardized biobehavioral assessment. Factors describing immunity, plasma cortisol, and emotion regulation were generated from these data using factor analysis. Paternal, but not maternal, NR was associated with greater emotionality and higher plasma cortisol, compared with infants born to CONTROL reared fathers.

Conclusions: These data suggest that macaque biobehavioral makeup is strongly influenced by paternal experiences, and via non-social mechanisms.

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References
1.
Capitanio J, Miller L, Schelegle E, Mendoza S, Mason W, Hyde D . Behavioral inhibition is associated with airway hyperresponsiveness but not atopy in a monkey model of asthma. Psychosom Med. 2011; 73(4):288-94. PMC: 3090450. DOI: 10.1097/PSY.0b013e3182155c83. View

2.
Kinnally E, Lyons L, Abel K, Mendoza S, Capitanio J . Effects of early experience and genotype on serotonin transporter regulation in infant rhesus macaques. Genes Brain Behav. 2007; 7(4):481-6. DOI: 10.1111/j.1601-183X.2007.00383.x. View

3.
Danese A, Moffitt T, Harrington H, Milne B, Polanczyk G, Pariante C . Adverse childhood experiences and adult risk factors for age-related disease: depression, inflammation, and clustering of metabolic risk markers. Arch Pediatr Adolesc Med. 2009; 163(12):1135-43. PMC: 3560401. DOI: 10.1001/archpediatrics.2009.214. View

4.
Mashoodh R, Franks B, Curley J, Champagne F . Paternal social enrichment effects on maternal behavior and offspring growth. Proc Natl Acad Sci U S A. 2012; 109 Suppl 2:17232-8. PMC: 3477388. DOI: 10.1073/pnas.1121083109. View

5.
McCormack K, Sanchez M, Bardi M, Maestripieri D . Maternal care patterns and behavioral development of rhesus macaque abused infants in the first 6 months of life. Dev Psychobiol. 2006; 48(7):537-50. DOI: 10.1002/dev.20157. View