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Broad, K. D., Curley, J. P., & Keverne, E. B. (2006). Mother-infant bonding and the evolution of mammalian social relationships. Phil. Trans. Biol. Sci., 361(1476), 2199–2214.
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. © 2006 The Royal Society.
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Brennan, P. A., & Kendrick, K. M. (2006). Mammalian social odours: attraction and individual recognition. Phil. Trans. Biol. Sci., 361(1476), 2061–2078.
Abstract: Mammalian social systems rely on signals passed between individuals conveying information including sex, reproductive status, individual identity, ownership, competitive ability and health status. Many of these signals take the form of complex mixtures of molecules sensed by chemosensory systems and have important influences on a variety of behaviours that are vital for reproductive success, such as parent-offspring attachment, mate choice and territorial marking. This article aims to review the nature of these chemosensory cues and the neural pathways mediating their physiological and behavioural effects. Despite the complexities of mammalian societies, there are instances where single molecules can act as classical pheromones attracting interest and approach behaviour. Chemosignals with relatively high volatility can be used to signal at a distance and are sensed by the main olfactory system. Most mammals also possess a vomeronasal system, which is specialized to detect relatively non-volatile chemosensory cues following direct contact. Single attractant molecules are sensed by highly specific receptors using a labelled line pathway. These act alongside more complex mixtures of signals that are required to signal individual identity. There are multiple sources of such individuality chemosignals, based on the highly polymorphic genes of the major histocompatibility complex (MHC) or lipocalins such as the mouse major urinary proteins. The individual profile of volatile components that make up an individual odour signature can be sensed by the main olfactory system, as the pattern of activity across an array of broadly tuned receptor types. In addition, the vomeronasal system can respond highly selectively to non-volatile peptide ligands associated with the MHC, acting at the V2r class of vomeronasal receptor.The ability to recognize individuals or their genetic relatedness plays an important role in mammalian social behaviour. Thus robust systems for olfactory learning and recognition of chemosensory individuality have evolved, often associated with major life events, such as mating, parturition or neonatal development. These forms of learning share common features, such as increased noradrenaline evoked by somatosensory stimulation, which results in neural changes at the level of the olfactory bulb. In the main olfactory bulb, these changes are likely to refine the pattern of activity in response to the learned odour, enhancing its discrimination from those of similar odours. In the accessory olfactory bulb, memory formation is hypothesized to involve a selective inhibition, which disrupts the transmission of the learned chemosignal from the mating male. Information from the main olfactory and vomeronasal systems is integrated at the level of the corticomedial amygdala, which forms the most important pathway by which social odours mediate their behavioural and physiological effects. Recent evidence suggests that this region may also play an important role in the learning and recognition of social chemosignals.
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Bernstein, I. S., & Dobrofsky, M. (1981). Compensatory social responses of older pigtailed monkeys to maternal separation. Dev Psychobiol, 14(2), 163–168.
Abstract: Thirteen 3-5-year-old pigtailed monkeys were subjected to five 2-hr maternal separations while remaining in their normal social group. Significant changes in activity profiles were noted during separation and reunion phases. This suggests the continued social dependence of older offspring upon the matriarch. The shift in social activities reflected attempts by the juvenile and adolescent subjects to compensate for maternal absence by intensification of other affiliative social behavior and avoidance of potentially socially disruptive situation. The subjects oriented more towards kin in the absence of the matriarch, but actual time with kin decreased. Upon the return of the matriarch, the intensified some responses depressed during her absence and returned to preseparation social relationships. Play and aggressive responses declined whereas social approaches increased during maternal absences. Submissive responses declined upon the return of the matriarch, and play increased. The subjects also showed a marked, temporary increase of direct interaction, largely sniffing and grooming, with the matriarch upon her return.
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Barber, J. A., & Crowell-Davis, S. L. (1994). Maternal behavior of Belgian (Equus caballus) mares. Appl. Anim. Behav. Sci., 41(3-4), 161–189.
Abstract: The relationship between ten Belgian mares and their offspring was studied from the first day of foal life to 17 weeks of age. Mares and foals spent more time at greater distances from each other as foals matured. Mares exhibited the recumbency response, being in closer proximity to their foals when foals were recumbent than when they were upright. Foals initiated the majority of nursing bouts. Frequency and duration of nursing bouts and percentage of time resting recumbently declined as foals matured. Foals also terminated the their foals, and they were most likely to do so in the first month of foal life. Maternal initiation of nursing. There was usually no discernible foal response to maternal aggression. Little difference between maternal behavior directed towards colts and fillies was found for all aspects of the study. Maternal behavior in the Belgian draft horse was similar to that reported for other equid breeds.
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Amdam, G. V., Csondes, A., Fondrk, M. K., & Page, R. E. J. (2006). Complex social behaviour derived from maternal reproductive traits. Nature, 439(7072), 76–78.
Abstract: A fundamental goal of sociobiology is to explain how complex social behaviour evolves, especially in social insects, the exemplars of social living. Although still the subject of much controversy, recent theoretical explanations have focused on the evolutionary origins of worker behaviour (assistance from daughters that remain in the nest and help their mother to reproduce) through expression of maternal care behaviour towards siblings. A key prediction of this evolutionary model is that traits involved in maternal care have been co-opted through heterochronous expression of maternal genes to result in sib-care, the hallmark of highly evolved social life in insects. A coupling of maternal behaviour to reproductive status evolved in solitary insects, and was a ready substrate for the evolution of worker-containing societies. Here we show that division of foraging labour among worker honey bees (Apis mellifera) is linked to the reproductive status of facultatively sterile females. We thereby identify the evolutionary origin of a widely expressed social-insect behavioural syndrome, and provide a direct demonstration of how variation in maternal reproductive traits gives rise to complex social behaviour in non-reproductive helpers.
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