The expression of father-daughter bond behaviors influences adult partner attachment in titi monkeys

Abstract

Abstract Coppery titi monkeys ( Plecturocebus cupreus ) are socially monogamous monkeys that display strong pair bonds similar to human romantic attachments, preceded by infant attachment to their fathers. To understand how father-daughter bonds impact adult relationship dynamics, we established a novel method for quantifying expression of bond-related behaviors. We assessed behavioral and neural correlates of preference, stress buffering, and separation distress to identify how females’ current and former attachment figures impact female attachment. Whereas all females ( n  = 9) shifted to preferring their partner over father six-months post-pairing, females that exhibited higher expression of juvenile parent preference maintained a relationship with their father six-months post-pairing, as evidenced by higher-than-expected father proximity. Higher expression of juvenile measures of proximity following a brief separation predicted slightly increased partner proximity in adulthood. Neural activity patterns in brain regions assessed pre- and post-pairing showed high similarity in glucose metabolism, despite overall activity being lower post-pairing. While there was some inconsistency in results, higher expression of juvenile proximity following a separation was associated with enhanced reduction in activity within social bonding brain regions (social salience network, periaqueductal gray, cerebellum), suggesting a potential stress buffering benefit via reduced threat-related brain activation, like that seen in high-quality human relationships. These findings advance current knowledge of how early relationships may shape adult bond-related behavior and neural activity.