Interdisciplinary perspectives on the principle of reciprocation

Abstract

Competition is at the heart of evolution (Darwin, 1859). Every individual to date has ancestors that were once more successful in passing their genes to the next generation than others. As a result, individuals should strive to outcompete others and perhaps to make their competitor's life even harder, for instance, by cheating on them. In such a competitive world, it might come as a surprise that across the phylogenetic tree individuals help others, including bacteria (Diggle et al., 2007), amoebae (Strassmann & Queller, 2011), insects (Field & Leadbeater, 2016), fishes (Frommen & Fischer, 2021), birds (Riehl, 2013), and our own species (Burton-Chellew et al., 2010) to name just a few examples.

Why would anyone help a potential rival? Theoretical work has shown that helping can lead to direct and indirect fitness benefits for the helper. For instance, helping kin might enable them to reproduce more often or to better care for their offspring. Because their offspring is genetically related to the helper, the helper gains indirect fitness benefits by transmitting shared genes to the succeeding generation (Hamilton, 1964). However, not all cooperation takes place between relatives, such as most of our own cooperative interactions occur between unrelated friends, workmates, or business partners. Here, indirect fitness gains cannot explain cooperation. However, helping others can also result in direct benefits, if previous recipients return the help in the future; this is called reciprocity (Trivers, 1971).

The significance of reciprocal cooperation to the functioning and stability of human societies has been recognised in many academic disciplines. Reciprocity is a widespread practice in our species (Bowles et al., 1997). It forms the basis for economic transaction and trade (Frank et al., 2018). As an ethical imperative, it is central to many world religions (Neusner & Chilton, 2008). Reciprocity is also a trait that emerges early in our ontogeny, as children at the age of 3 years reliably reciprocate (Warneken & Tomasello, 2013), suggesting evolutionary conservation (Warneken & Tomasello, 2009). Further, it has been described in human foragers (Jaeggi & Gurven, 2013), whose socio-ecology is probably closest to the conditions of early humans (Tooby & Cosmides, 2015).

Even though reciprocity seems ubiquitous and significant in our species, its proximate mechanisms and ultimate causes are still not well understood. The purpose of this special issue is to explore the principle of reciprocity in a diverse way by employing theoretical and empirical research as well as presenting observational and experimental evidence while featuring a multitude of species from invertebrates to humans. In the following, I will present some of the key findings from reading the contributions.

It is debated whether reciprocity predates our species and can be found in other animals (Hammerstein, 2003). Early studies, such as those on food sharing in vampire bats, Desmodus rotundus (Wilkinson, 1984) or predator inspection in sticklebacks, Gasterosteus aculeatus (Milinski, 1987) initially became famous examples of non-human reciprocal cooperation. Yet, soon after discovery, these classic examples were contested as being confounded and not providing sufficient evidence (Clutton-Brock, 2009; Connor, 1986; Noë, 2006; Paolucci et al., 2006). An article in this special issue revisits reciprocal predator inspection, a former textbook example for reciprocity (Veiros et al., 2024). By critically reviewing the available literature, the authors conclude that there is evidence for predator inspection being contingent on the partner's behaviour and predator's presence in several fish species. They offer future avenues and suggest that remaining controversies can be addressed with new technology, such as automatic tracking, and advanced analyses, such as machine learning, that has become recently available and affordable (cf. Jungwirth et al., 2021). Yet, some alternative explanations for reciprocal help are more difficult to deal with empirically. One of these is called pseudo-reciprocity (Bshary & Bergmüller, 2008; Connor, 1995), where a cooperative individual receives a reciprocal return as a by-product of their donation. This stands in contrast to ‘true’ reciprocity where a cooperative individual receives a reciprocal return as a reward for their donation. In this special issue, Carter argues in a thoughtful opinion piece that both forms of exchange can coexist in a continuum and that it is more useful to study their relative contribution on received and given help to understand the importance of reciprocity more generally (Carter, 2024).

One argument for why reciprocity might not be common in animals other than our own species is its assumed dependence on sophisticated cognition (Stevens et al., 2005; Stevens & Hauser, 2004). Indeed, it is widely believed that reciprocity is too cognitively demanding to exist in non-human species (Clutton-Brock, 2009; Hauser et al., 2009; McAuliffe & Thornton, 2015). Yet, this special issue provides convincing evidence for reciprocity in species with different cognitive skill sets. First, Schino and colleagues show that Himalayan thar (Hemitragus jemlahicus) reciprocate grooming not only immediately but also over prolonged time scales (Schino et al., 2024). The authors argue that rather than an explicit understanding of cost–benefit calculations, there are less cognitively demanding mechanisms such as emotions underlying thar's reciprocal actions (reviewed in Schino & Aureli, 2010; Schweinfurth & Call, 2019a). Second, a meta-analysis on food-provisioning in Norway rats (Rattus norvegicus) showed that rats share food readily and reciprocally with others (Engelhardt & Taborsky, 2024). The rats help conspecifics who helped them in the past, following a ‘You helped me, so I help you’ rule. Females, but not males, also sometimes use the cognitively simpler rule of thumb ‘You helped me, so I help anyone’. This generalised form of reciprocity is interesting because it can lead to stable levels of cooperation (Pfeiffer et al., 2005) without requiring individual recognition, thereby reducing cognitive demands. Finally, robust reciprocal cooperation was found in a small polychaete worm, even when their interactions were disturbed (Lorenzi et al., 2024). These hermaphrodite worms (Ophryotrocha diadema) can produce both sperm and eggs. Since producing eggs is more energetically costly, mating in the male function is preferred. Yet, they require a partner in the female function to reproduce. To solve the issue, they take turns and trade eggs with sperms (Picchi et al., 2018). This reciprocal exchange apparently does not even require a brain.

These findings suggest humans are not unique in their ability to exchange commodities and services reciprocally. Perhaps, reciprocity evolved in humans separately compared to other animals. Cross-species comparisons can examine similarities and differences, which can inform us about evolutionary ancestry. Good candidates for comparisons are members of our own taxonomic order – other primates. A comparative study on humans and one of our closest-living relative, the chimpanzee (Pan troglodytes; Perelman et al., 2011), revealed that both species reciprocated help when presented with the same task, although the effect was less pronounced in chimpanzees (Knofe et al., 2024). This suggests that reciprocity might have originated in at least a common ancestor. Furthermore, a different form of reciprocity was described in Barbary macaques (Macaca sylvanus), a more distantly related primate species (Schülke et al., 2024). Reciprocity can take a positive ‘Reward kindness with kindness’, but also a negative ‘An eye for an eye’ form (cf. Guevara Beltran et al., 2023). The macaques show a mix of both when supporting others during fights. Males are more likely to support males who are loyal to them by not attacking them in fights. Such strategic alliances are remarkable as they show how complex the principle of reciprocity can be (Schülke et al., 2024).

It is important to note that not all studies reported here provide evidence for reciprocity in non-human animals. Nevertheless, much can be learned from these findings. For instance, dogs did not provide more food to a helpful compared to an unhelpful conspecific partner in an experimental food-provisioning task (McGetrick et al., 2024). This stands not only in contrast to the principle of reciprocity but also in seemingly contrast to earlier findings (Gfrerer & Taborsky, 2017, 2018; McGetrick & Range, 2018). Yet, the dogs did also not consider the presence or absence of a partner when pressing a button to provide food. The authors argue that this suggests that the dogs might have not fully understood the task, which could explain the conflicting finding. This highlights the importance of conducting task understanding controls alongside the main experiment when investigating cognitive abilities (cf. Brosnan, 2017; Schweinfurth & Call, 2019b). Another study investigated reciprocity in a group-provisioning task in three corvid species and found an effect of previously received help by conspecifics in only a handful of dyads (Horn et al., 2024). This suggests no evidence for reciprocity at the group level, which is inconsistent with earlier findings in one of the tested species (Fraser & Bugnyar, 2012; Müller et al., 2017). The authors propose that not being able to select certain partners as recipients of help in a group setting could have impacted the likelihood to find reciprocity in their study. Future research should compare dyadic with group settings to understand the role of partner choice in reciprocating help. In line with this argument, a review in this special issue demonstrates that the social setting and the identity of the recipient of help appears crucial for successful reciprocal interactions (Brosnan, 2024). Despite the initial absence of evidence supporting reciprocity, these studies present a great opportunity to learn more about the principle of reciprocity as they enable us to explore under which conditions reciprocity is more likely to be exhibited.

Astonishingly, many unresolved questions persist regarding reciprocity in our own species despite decades of empirical and theoretical research as illustrated in a comprehensive review article of this special issue (Rossetti & Hilbe, 2024). The authors argue, for instance, that reciprocity has been mainly studied in computerised and standardised tasks, such as the iterated Prisoner's Dilemma. Yet, our typical cooperative interactions involve partners of different relationships, such as friends or strangers, that can drastically affect reciprocal levels. Furthermore, the authors show that models are not always successful in predicting real strategies, suggesting an important mismatch between both. In addition, cognitive challenges affect us, too, and knowledge on the proximate mechanisms of human reciprocity is remarkably limited. As a result, it is not clear how we cooperate in large, complex, and interconnected societies where a considerable amount of information needs to be memorised to reciprocate help reliably. Moreover, we monitor not only our own interactions with others but also help those who have the reputation of being cooperative (Milinski et al., 2002; Nowak & Sigmund, 2005). However, a theoretical model reported in this special issue challenges the role of reputations in third-party reciprocal interactions (Roberts, 2024). Roberts proposes instead that indirect fitness benefits due to structured populations could explain third-party helping and that future work should focus on the role of culture on reciprocal helping.

Finally, this special issue illustrates that the principle of reciprocity is of importance to multiple academic fields because it attracted contributions from Animal Cognition, Behavioural Ecology, Comparative Psychology, Evolutionary Anthropology, Mathematical Biology, and Social Economics. Although the principle of reciprocity seems simple at first sight, this special issue shows that it is more complex and multifaceted when taking a second look. I believe this is why there are so many disciplines that have been concerned with the principle for decades. While interdisciplinary communication is certainly not trivial, it is a unique opportunity to cross-pollinate ideas, which will enable us to develop new theories and methodologies and eventually to gain a more holistic understanding.

In conclusion, the principle of reciprocity is a highly contested claim that is acknowledged as powerful and widespread by some and rejected as rare and complex by others. This special issue provides evidence for reciprocity across the phylogenetic tree. Further, rather than assessing its presence in empirical and theoretical studies, this issue went beyond the current state of knowledge by integrating controversies to investigate the intricate mechanisms and causes of reciprocity. There is still much to learn about the complexities of reciprocity, and I hope this special issue will stimulate future research.

Manon K. Schweinfurth: Writing – original draft.

This work was supported by the Biotechnology and Biological Sciences Research Council (grant number: BB/X00631X/1).