Abstract
A μ-opioid receptor (OPRM1) single-nucleotide-polymorphism, found in both humans and rhesus macaques mediates the mother-infant attachment bond. Because mothers treat their sons and daughters differently, it is somewhat surprising that the role of infant sex has not been assessed in the context of a maternal-OPRM1-genotype-by-infant-sex interaction. The present study investigates the effect of maternal-OPRM1-genotype and infant sex on mother-infant behaviors. Over the first 6 months of offspring life, mother-infant behavioral data assessing attachment quality was collected twice weekly from a large number of rhesus monkey mother-infant pairs (N = 161 dyads; n = 64 female infants, n = 97 male infants). Mothers were genotyped for OPRM1 variation. Factor analysis of the observed behaviors showed two factors: Attachment (maternal-infant cradling, rejections, and infant approaches and leaves), and Maternal Restraints (mother restrains infant, preventing exploration). Further analyses showed a two-way, maternal-genotype-by-infant-sex interaction for both factors. For Attachment, mothers with the CC genotype cradled and restrained (Maternal Restraints) their female infants more and rejected them less, when compared to female infants of CG mothers. Perhaps as a consequence, female infants of CC genotype mothers approached and left their mothers less often, when compared to female infants of CG mothers, likely an indication that female infants from mothers with CG genotype play a greater role in maintaining the mother-infant bond than do female infants from CC genotype mothers. This finding may also indicate a more secure attachment in infants from CC genotype mothers. Unlike female infants, on average, the mother-infant relationship of dyads with a male infant was largely undifferentiated by maternal genotype. These findings suggest that, in contrast to female infants from CG mothers, CC mothers and their female infants appear to have a closer mother-infant relationship which may portend close life-long bonds, as mothers and female offspring remain together throughout life. Male offspring appear to have a more aloof mother-infant bond regardless of OPRM1-genotype. The results of this study indicate that maternal-OPRM1 variation mediates mother-infant attachment behaviors for female infants and has less effect for male infants. This suggests that offspring sex should be included in studies investigating the effect of maternal-OPRM1 genotype on the mother-infant attachment relationship.
Highlights
Mothers of infant daughters talk to and look more often at their female infants (Lewis, 1972, p. 106), which may be a function of the infants’ behaviors, with female infants showing higher rates of vocalizations and more time looking at their mothers
This study focuses on the effects of maternal-OPRM1 genotype and infant sex on mother-infant behavior over the first 5 months of infant life, assessing mother-infant behaviors that characterize attachment and independence
The results indicated that mothers that possessed the CC genotype showed evidence of a more engaged mother-infant bond with their daughters as indicated by their Attachment factor scores, when compared to CG mothers and their female infants
Summary
The mother-infant bond is necessary for survival, but critical to the normative development of the complex primate brain. In Maccoby and Jacklin’s (1978) classic monograph of sex differences, they critically review findings showing that male and female infants behave differently beginning early in life. They conclude that infant males are more active, aggressive, and independent than females. When the two sexes were compared in one study (Connellan et al, 2000), male neonates exhibited a stronger interest in a physical-mechanical mobile, whereas female infants showed greater interest in a face (but see Maylott et al, 2021). In non-human primates, female infants reared in a neonatal nursery, where they have no experience with adult monkeys, look longer at computer generated faces and engage in more social affiliative behaviors with their human caregivers than males (Simpson et al, 2016). Male infants’ greater overall activity, increased rates of play ( rough and tumble play), and higher rates of aggression could affect maternal behaviors, leading to differential treatment of sons and daughters
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