Mother–infant bonding and the evolution of mammalian social relationships

Abstract

A wide variety of maternal, social and sexual bonding strategies have been described across mammalian species, including humans. Many of the neural and hormonal mechanisms that underpin the formation and maintenance of these bonds demonstrate a considerable degree of evolutionary conservation across a representative range of these species. However, there is also a considerable degree of diversity in both the way these mechanisms are activated and in the behavioural responses that result. In the majority of small-brained mammals (including rodents), the formation of a maternal or partner preference bond requires individual recognition by olfactory cues, activation of neural mechanisms concerned with social reward by these cues and gender-specific hormonal priming for behavioural output. With the evolutionary increase of neocortex seen in monkeys and apes, there has been a corresponding increase in the complexity of social relationships and bonding strategies together with a significant redundancy in hormonal priming for motivated behaviour. Olfactory recognition and olfactory inputs to areas of the brain concerned with social reward are downregulated and recognition is based on integration of multimodal sensory cues requiring an expanded neocortex, particularly the association cortex. This emancipation from olfactory and hormonal determinants of bonding has been succeeded by the increased importance of social learning that is necessitated by living in a complex social world and, especially in humans, a world that is dominated by cultural inheritance.

Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees

“…In mammals, lactation has been described as the primary form of food sharing [73], and is well known to be connected to peripheral and central oxytocin release in mammals [34,74]. This positive feedback circuitry is considered a key mechanism for bond formation between mother and infant [34,75]. In some mammals, maternal care Table 4.…”

Oxytocin is associated with infant-care behavior and motivation in cooperatively breeding marmoset monkeys

“…Its ancient functions in female reproduction, related to cervix and uterus distension during labor (Blanks and Thornton, 2003;Kendrick and Keverne, 1989;Landgraf et al, 1983;Nissen et al, 1995), milk injection during lactation (Uvnäs-Moberg et al, 2001), and the regulation of maternal behavior (Feldman, 2007;Kendrick, 2000;Kendrick et al, 1987;Pedersen et al, 1994;Uvnäs-Moberg, 1996), probably formed the basis for derived OT functions in non-maternal social contexts (Broad et al, 2006;Kendrick, 2000;Lim and Young, 2006). However, less is known about the role of OT in alloparental care, i.e.…”

Sex differences in learning the allocation of social grooming in infant stumptailed macaques

“…Keverne et al (1996) and Broad et al (2006) have proposed that the mammalian brain evolved to favour mother-offspring attachment (sensu Bowlby, 1969Bowlby, , 1973. In primates, learning to make decisions via maternal examples may account for the enlargement of the neocortex (Keverne et al, 1996); a conclusion also reached by Joffe (1997) with regards to the primate extended juvenile period.…”