Oxytocin modulates mate-guarding behavior in marmoset monkeys

Abstract

In socially-monogamous species, intolerance of interactions between a pairmate and a sexual rival (i.e., mate-guarding) promotes the preservation of long-lasting partnerships. One promising neurobiological candidate for the regulation of mate-guarding behavior in monogamous primates is the oxytocin (OT) system, given its established role in both the development of monogamous bonds and the behavioral processes that facilitate the preservation of those bonds. In this study, male and female marmosets were exposed to a same-sex intruder in their home environment during conditions when their pairmate was present and absent, and across three treatment conditions (OT receptor agonist; saline control; OT receptor antagonist). Saline-treated marmosets spent significantly more time in proximity to the intruder, relative to the empty pairmate enclosure, when their pairmate was absent. However, when marmosets received OT they spent less time in proximity to the intruder, indicating that OT may reduce interest in a same-sex stranger in a territorial context. When their pairmate was present, saline-treated marmosets spent equal time in proximity to both intruder and pairmate; yet when they received OT they spent significantly more time in proximity to the intruder, indicating that OT may increase interest in a same-sex stranger in a mate-guarding context. While OT treatment did not directly influence the expression of aggression, OT system manipulations impacted the expression of selective social interest during an intruder challenge, suggesting that OT may enhance adaptive responses to social challenges. Moreover, these findings add to the converging evidence that the OT system regulates behavioral processes that underlie the preservation of established relationships.

Keywords: Aggression; L-368,899®; Mate-guarding; Monogamy; Oxytocin; Pairbond; Primates; Pro(8)-OT; Sociality.

Figure 1.

Design of the intruder challenge is displayed [subject=black; pairmate=dark grey; intruder=light grey]. In the intruder trials, subjects received three drug treatments [oxytocin receptor agonist Pro⁸-OT; oxytocin receptor antagonist (OTA: L368,899); saline control] across two pairmate presence conditions [pairmate present; pairmate absent]. In the two intruder-absent control trials, the procedure was the same as above except the intruder (light grey) was not present for either pairmate present or pairmate absent conditions and subjects received saline.

Figure 2.

Mean (± SEM) duration of time spent in proximity to the pairmate enclosure and intruder enclosure, during (A) pairmate absent and (B) pairmate present conditions, are expressed as a function of OT treatment. Marmosets were treated with OT receptor agonist (OT), OT receptor antagonist (OTA), and saline control (SAL) during conditions when the intruder was present, and saline control (SAL – hatched bars) when the intruder was absent. Letters and asterisks indicate significant differences (a > b > c > d at p < 0.05, * at p < 0.05, ^# at p < 0.1). Data points from individual marmosets are displayed for each condition (♦; n=8).

Figure 3.

Mean (± SEM) (A) frequency and (B) and duration of time spent interacting with the pairmate enclosure and intruder enclosure are expressed as a function of OT treatment. Marmosets were treated with OT receptor agonist (OT), OT receptor antagonist (OTA), and saline control (SAL) during conditions when the intruder was present, and saline control (SAL – hatched bars) when the intruder was absent. Letters and asterisks indicate significant differences (a > b > c > d at p < 0.05, * at p < 0.05, ^# at p < 0.1). Data points from individual marmosets are displayed for each condition (♦; n=8).

Figure 4.

Mean (± SEM) values for social behaviors directed at the pairmate enclosure and the intruder enclosure are expressed as a function of pairmate presence. (A) Time spent per proximity bout, (B) interaction index, (C) latency to first aggression, and (D) aggression frequency, are presented. Interaction index (B) scores range from −1 to +1; where a positive score indicates that marmosets spent a greater proportion of their time directly interacting with the pairmate enclosure compared to the intruder enclosure and a negative score indicates that marmosets spent a greater proportion of their time directly interacting with the intruder enclosure compared to the pairmate enclosure. Letters indicate significant differences (a > b at p < 0.05, ^# at p < 0.1). Data points from individual marmosets are displayed for each condition (♦; n=8).

Figure 5.

Mean (± SEM) cortisol and testosterone levels the morning of the intruder challenge (pre-exposure) and the morning after the intruder challenge (post-exposure). Data are expressed as a function of pairmate presence (A and C) and OT-treatment (B and D). Marmosets were treated with OT receptor agonist (OT), OT receptor antagonist (OTA), and saline control (SAL) during conditions when the intruder was present, and saline control (SAL – hatched bars) when the intruder was absent. Asterisks indicate significant differences at p < 0.05. Data points from individual marmosets are displayed for each condition (♦; n=8).