Oxytocin-like receptors mediate pair bonding in a socially monogamous songbird

Abstract

Although many species form socially monogamous pair bonds, relevant neural mechanisms have been described for only a single species, the prairie vole (Microtus ochrogaster). In this species, pair bonding is strongly dependent upon the nonapeptides oxytocin (OT) and vasopressin, in females and males, respectively. Because monogamy has evolved many times in multiple lineages, data from additional species are required to determine whether similar peptide mechanisms modulate bonding when monogamy evolves independently. Here we test the hypothesis that OT-like receptor activation is required for pair bond formation in the socially monogamous zebra finch (Taeniopygia guttata). Males and females were administered chronic intracerebroventricular infusions of saline or an OT receptor antagonist and were observed twice daily for 3 days in a colony environment. A variety of affiliative, aggressive and other behaviours were quantified. The antagonist produced significant and selective effects on pair bonding (latency to pair; number of sessions paired; stable pairing) and the associated behaviour of allopreening. Importantly, findings for males follow the trends of females; this yields main effects of treatment in two-way ANOVAs, although within-sex analyses are significant only for females. These data provide evidence for both convergent evolution and species diversity in the neuroendocrine mechanisms of pair bonding.

Hypothalamic oxytocin and vasopressin neurons exert sex-specific effects on pair bonding, gregariousness, and aggression in finches

“…For example, activation of OTRs, but not V1aRs, is necessary for the establishment of pair bonds in zebra finches, with much stronger effects in females (16,19,26). Similarly, pair bonding in female prairie voles is more strongly dependent on OTR activation than on V1aR activation, whereas the converse is true for males (27).…”

“…OTR antagonism also reduces the preference for the larger of two groups, impairs pair bonding, and reduces the preference for familiar same-sex birds. These effects are significantly stronger in females (18,19). We initially hypothesized that the antagonist effects on gregariousness and pair bonding reflect endogenous release from VP neurons in the medial bed nucleus of the stria terminalis (BSTm), given that those neurons increase their transcriptional (Fos) activity selectively in response to positive, affiliation-related stimuli (1).…”

Empathy as a driver of prosocial behaviour: highly conserved neurobehavioural mechanisms across species

“…OT-like neuropeptides have played special roles in social affiliation and reproduction ever since the peptides first evolved (450 Ma), and exert widespread influences on affiliative behaviours across a variety of vertebrate classes [24]. For instance, studies have demonstrated that endogenous activation of oxytocic receptors in the brain is necessary for the natural formation of pair bonds in zebra finches [25], as has previously been shown in prairie voles [26]. An analysis of the role of OT suggests that its peripheral role is in smooth-muscle contraction, specifically in uterine contractions and lactation, and has been co-opted to serve in organizing and coordinating maternal care and motheroffspring bonding.…”

Long-life partners or sex friends? Impact of parental pair bond on offspring personality

“…Moreover, yolk oestrogens, progesterone and corticosterone can also influence offspring development (Hayward and Wingfield, 2004;Groothuis et al, 2005;Gil, 2008;Henriksen et al, 2011). In this study, we hypothesize the involvement of mesotocin and vasotocin, homologues of mammalian oxytocin and vasopressin (Klatt and Goodson, 2013;Pedersen and Tomaszycki, 2012), in these prenatal effects. As the formation of bird pair bonds appears to be modulated by mesotocin and vasotocin, we reasonably suggest that our two sets of quail did not present the same levels of these nonapeptides.…”