Interdependence and the cooperative breeding system: insights from captive and wild common marmosets (Callithrix jacchus)

Abstract

The human social repertoire is one of the most puzzling phenomena and historically under examination by several philosophical and scientific traditions. Both the extent of that repertoire and the evolutionary process that fostered such a complex system are of particular interest for behavioural anthropologists. From this school of thought emerges a notable hypothesis tackling the evolution of our social behaviour, the cooperative breeding hypothesis (CBH). Cooperative breeding systems are present in group living species in which offspring receive extensive care from individuals other than their parents. Moreover, because of the prevalence of parental and, especially, alloparental care, this system is also characterized by life history attributes as well as behavioural peculiarities. The CBH posits that, under naturalistic conditions, the psychological and motivational mechanisms required for a cooperative breeding system to function smoothly might also support an increase in performance in a variety of socio-cognitive contexts and tasks. My approach was to explore the behavioural variation associated to contrasting interdependence levels in a cooperatively breeding primate species, namely the common marmoset (Callithrix jacchus). Interdependence, a concept referring to the situation that a subject impacts a conspecifics’ overall fitness, is generally high in cooperative breeders, but variation also exists. Hence, comparing intraspecific behavioral variation in marmosets under different levels of interdependence allows for valuable insights into the underpinnings of their cooperative breeding system. These insights have implications for our understanding of the evolution of the human social repertoire and further tests of the CBH. The overarching goal of my PhD thesis was to investigate the CBH by exploring interdependence-driven intra-specific behavioural variation. In the first three subsequent empirical chapters, I assessed C. jacchus’ behavioural outputs by looking into three biologically relevant behaviours, namely social tolerance, food sharing and reaction to conspecific’s distress. Lastly, I reviewed the cooperative breeding system by addressing its prevalent definitions and pitfalls, the ecological benefits to parents, offspring, and helpers, the possible evolutionary pathways for this system to emerge and thrive, and finally, the behavioural consequences of the cooperative breeding system. In chapter 2, my goal was to assess if common marmosets’ social tolerance is higher in captivity where food is readily available or in the more demanding wild setting. The main finding was that, unlike independently breeding primates, adult common marmosets displayed higher social tolerance toward each other in the wild setting where food is scarce and mutual interdependence to successfully raise offspring therefore high. The results in this chapter thus emphasize the crucial relevance of interdependence in the evolution of highly tolerant cooperative breeders and therefore has implications for our understanding of the origins of humans’ social tolerance and hyper-cooperation. In chapter 3, the goal was to investigate how wild-living C. jacchus adjust their foodsharing behaviour towards infants as food availability varies. The primary finding was that all common marmosets, except female helpers, engage in an interdependence-driven strategy in which decreasing food availability increases food-sharing behaviour toward infants; this was also the case for older infants and for hard to obtain food items. Despite playing a relevant role overall in infant care, female helpers engage in an ecologically driven strategy and thus share food to infants more often when food is more abundant. This chapter helps us to illustrate how C. jacchus’ behavioural variation is remarkably reliant on interdependence levels. Additionally, it consolidates the interconnection between the cooperative breeding and interdependence hypothesis and their role in the evolution of the cooperative breeding system. Finally, in chapter 4, the ultimate objective was to evaluate how common marmosets react to conspecifics in distress and try to disentangle if emphatic rather than selfish motivations would govern these reactions. I found that all group members displayed contagion of emotional arousal, a previously unknown behaviour in common marmosets, thus indicating that common marmosets have a larger social repertoire than previously thought. Furthermore, I also found that male individuals were more likely to approach conspecifics in distress than relaxed ones, a finding consistent with the more conspicuous proactive prosociality from male common marmosets. Altogether, these results from chapter 4 highlight C. jacchus’ empathic competence in light of the combination model framework and helps us to better explain the emergence of empathetic capacities by moving the spotlight from large-brained species to highly interdependent ones. Overall, the main findings from this thesis reflect how interdependence is a driving force for social tolerance and food sharing in the cooperatively breeding common marmoset. Moreover, they also support the importance of social environments shaped through reproductive interdependence for the evolution of complex social skills in our model species, without the presence of large brains and its ensuing computational potency. Notably, the underlying finding from my thesis is the usefulness of interdependence variation as a tool to manipulate and thus expand our comprehension regarding the cooperative breeding system. Furthermore, interdependence appears to work as a linchpin for the cooperative breeding system, and therefore, its controlled manipulation might be used to assess a whole host of behavioural outputs from other species under this system and further explore the cooperative breeding intricacies.