The investigation of prosocial behavior (i.e. voluntary actions that benefit another individual at no or low costs to the actor; Marshall-Pescini et al., 2016), is of particular interest from an evolutionary point of view, because the act of benefitting another individual without receiving a direct gain to oneself represents an evolutionary puzzle (Clutton-Brock, 2009; Riehl, 2013). Humans show high levels of prosocial behaviors from an early age on (Silk and House, 2011), although their expression and developmental trajectories are subject to cross-cultural and societal variation (House et al., 2020). The importance of prosociality for human interactions has inspired comparative studies on the evolutionary origin of this trait. The majority of experimental studies in non-human animals have focused on primates (for a review, see Marshall-Pescini et al., 2016), but recent research revealed prosocial tendencies also in other mammals (e.g. domestic dogs [Quervel-Chaumette et al., 2016]; wolves [Dale et al., 2019]; rats [Ben-Ami Bartal et al., 2011; Schweinfurth and Taborsky, 2018a]) and several bird species (e.g. azure-winged magpies [Horn et al., 2016; Massen et al., 2020]; pinyon jays [Duque et al., 2018]; African grey parrots [Brucks and von Bayern, 2020]). Nevertheless, not all tested species have shown prosocial tendencies (e.g. chimpanzees [Silk et al., 2005]; cottontop tamarins [Cronin et al., 2009]; meerkats [Amici et al., 2017]; common ravens [Di Lascio et al., 2013; Lambert et al., 2017; Massen et al., 2015a]). Following these variable initial results, the importance of understanding which social factors and which characteristics of a species’ social system may underlie the expression of prosociality across non-human animal species became particularly evident. Unfortunately, however, comparisons of prosociality across species have been hampered by the diversity of paradigms and procedures used (Marshall-Pescini et al., 2016).

The most comprehensive experimental investigation of prosocial behavior in primates tested 15 species (including human children) in the same experimental set up, that is the group service paradigm (hereafter GSP; Burkart et al., 2014). In the GSP, individuals are tested in their regular social group and can make food available to other group members by operating a simple mechanism, without obtaining any food themselves. Burkart et al., 2014 showed that species-specific prosocial tendencies in the GSP were best explained by the degree of allomaternal care (i.e. offspring care by individuals other than the mother) across the tested species. These results were in line with the cooperative breeding hypothesis, which states that ‘cooperative breeding is accompanied by psychological changes leading to greater prosociality’ (Burkart et al., 2009). Additional factors positively influencing the amount of prosocial behavior – albeit to a lesser degree than allomaternal care – were the presence of monogamous pair bonds and high social tolerance (i.e. equal access to food for all group members) measured during the GSP (Burkart et al., 2014). The latter result fits the self-domestication hypothesis (Hare et al., 2012; Hare, 2017), according to which prosociality arises as a by-product of selection against reactive aggression – particularly in males (Wrangham, 2019) – and selection for increased tolerance (see Sánchez‐Villagra and van Schaik, 2019 for a critical appraisal of historical and current theories on self-domestication). While both the cooperative breeding hypothesis and the self-domestication hypothesis acknowledge an underlying link between increased social tolerance and prosociality, the cooperative breeding hypothesis puts emphasis on allomaternal offspring care, whereas the self-domestication hypothesis suggests the decrease of reactive aggression as the crucial factor for the emergence of human-like prosociality. The comparative approach is particularly promising for distinguishing between these hypotheses (Burkart et al., 2014). However, concentrating solely on the primate order offers only one perspective on the evolution of prosocial behavior, which has also been criticized because of possible effects of common ancestry (e.g. cooperative breeding in primates occurs only in two taxonomic groups – humans and callitrichid monkeys; Thornton and McAuliffe, 2015). Hence, applying a standardized comparative approach to other taxonomic groups would be paramount for drawing more general conclusions (Beran et al., 2014).

From a comparative perspective, the corvid family, which is a cosmopolitan bird taxon that includes crows, ravens, jays, and magpies, is of particular interest for the investigation of prosociality. Corvids have similar neuron counts compared to many primate species (Olkowicz et al., 2016) and show similarly complex cognitive traits (Taylor, 2014; Güntürkün and Bugnyar, 2016; Boucherie et al., 2019). Most corvid species are long-lived, highly social (Emery et al., 2007) and pair bonds are extremely strong, even lifelong in some species (Henderson et al., 2000). About 40% of all extant corvid species from several separate genera are cooperative breeders (defined in birds as more than the two parents caring for the brood; for example azure-winged magpies, carrion crows; see Cockburn, 2006; Griesser et al., 2017). Since related as well as unrelated helpers have been documented to contribute to offspring care, both kin selection (Green et al., 2016) and pay-to-stay strategies (Kingma, 2017) seem important to explain cooperative breeding in birds. Additionally, a number of corvids breed colonially, where several pairs nest in physical proximity, including rooks, Eurasian jackdaws, and azure-winged magpies (see Madge and Burn, 1999). It has been argued that relaxed territorial defense, reduced reactive aggression, and increased tolerance toward conspecifics may lead to the emergence of colonial nesting in birds (Brown, 1974). Consequently, corvids’ variation in cooperative breeding and colonial nesting make them the optimal candidates for testing both the cooperative breeding hypothesis and the self-domestication hypothesis in a lineage other than primates.

Previous experiments in corvids have demonstrated prosocial behavior in azure-winged magpies (using the GSP Horn et al., 2016 as well as an active food-sharing paradigm Massen et al., 2020) and pinyon jays (using a prosocial choice task Duque et al., 2018). Both species breed cooperatively (Cockburn, 2006) and nest in colonies, with several breeding pairs nesting in close proximity (Madge and Burn, 1999). Additionally, there has been tentative evidence for prosocial tendencies in a prosocial choice task in Eurasian jackdaws (Schwab et al., 2012), which also nest in colonies, but do not breed cooperatively (Cockburn, 2006). In contrast, subadult ravens for example, which are able to cooperate with a conspecific partner to receive mutual rewards (Massen et al., 2015b; Asakawa-Haas et al., 2016), have so far not shown any evidence of prosociality, despite having been tested with multiple experimental paradigms (e.g. different prosocial choice tasks [Di Lascio et al., 2013; Lambert et al., 2017]; token exchange task [Massen et al., 2015a]). While ravens tend to form groups for foraging and roosting as non-breeders (Heinrich, 1989; Loretto et al., 2016), they are highly territorial during breeding (Boucherie et al., 2019) and it is not clear whether the characteristics of their social system contribute to their apparent lack of prosocial tendencies. To disentangle the influence of cooperative breeding and colonial/territorial nesting, respectively, on prosociality, it is necessary to test a sample of different species that vary along these factors, and to avoid differences that result from methodological heterogeneity by using the same standardized procedure.

Here, we present the first systematic comparison of prosocial behavior across multiple species in a taxonomic group outside the primate order. We measured prosociality in 11 social groups of eight corvid species (total N = 72 individuals), which were all highly social (i.e. living and foraging in social groups during at least some stages of their life history; Komeda et al., 1987; Uhl et al., 2019; Kubitza et al., 2015; Clayton and Emery, 2007; Braun et al., 2012; Miyazawa et al., 2020; Holzhaider et al., 2011; Ekman and Griesser, 2016), but varied in the expression of cooperative breeding and colonial nesting (Figure 1d). We used a standardized experimental paradigm developed in primates (i.e. the GSP; Burkart et al., 2014), which has recently been adapted and successfully applied in birds (Horn et al., 2016). To keep the results comparable, we kept the procedures as similar as possible to the original study with primates (Burkart et al., 2014). In the prosocial test of the GSP, individuals can land on the provisioning perch of the apparatus, and consequently make food available to their group members via a seesaw mechanism (Figure 1a). Crucially, the bird on the provisioning perch cannot obtain any food itself and it has to remain on the provisioning perch until another individual arrives on the other side of the apparatus (position 1; see Figure 1b) to take the food (see Video 1; see Materials and methods section for details). Habituation, training and two control conditions (i.e. empty control: no food available; blocked control: access to food blocked; see Video 2 and Video 3) ascertain that the individuals understand the experimental task and that landing on the provisioning perch in the prosocial test does not reflect the absence of sufficient inhibitory control (Figure 1c). In addition to prosocial tendencies, the GSP also measures how even the access to sequentially provided food is across the individuals of a given social group (i.e. whether one or few individuals monopolize the food source and obtain most of the food or whether similar numbers of food pieces are obtained by all group members; Figure 1c). In primates, this evenness score has been used as a proxy for social tolerance (Burkart et al., 2014).

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To assess the explanatory value of cooperative breeding and colonial nesting for prosocial behavior in corvids, we used linear regression models and an information-theoretic approach to model selection and model averaging. Additionally, since sex differences have been observed in prosocial food sharing in natural observations (von Bayern et al., 2007; Scheid et al., 2008; Chiarati et al., 2011) and experiments (Schwab et al., 2012), we also included the individuals’ sex into the model. Further, to test the extent to which common ancestry affected the birds’ prosocial tendencies, we calculated a phylogenetically controlled mixed-effects model (for phylogenetic relationships between the tested species, see Figure 1—figure supplement 1). Finally, because within a species prosocial behavior might be expressed differently between the sexes (Massen et al., 2020; Schwab et al., 2012; von Bayern et al., 2007) and between age classes (Chiarati et al., 2011), we also examined intraspecific provisioning patterns.

Our results demonstrate that cooperative breeding is positively associated with the expression of prosocial behavior in corvids, although this effect is qualified by interactions between sex and both the factors cooperative breeding and colonial nesting, which were also important for explaining the occurrence of prosocial behavior in the birds. Additional separate analyses for the two sexes showed that both cooperative breeding and colonial nesting positively affected prosociality, albeit differently for the two sexes. While the effect of cooperative breeding seemed to be driven by females’ prosociality, colonial nesting only predicted males’ prosocial actions. The phylogenetically controlled model confirmed the importance of both cooperative breeding and colonial nesting and showed that the phylogenetic signal was weak in terms of prosocial behaviors in corvids. Same-sex provisioning dyads were equally common as opposite-sex dyads and we observed both provisioning from adults to juveniles and vice versa. Our results highlight that both alloparental care and increased social tolerance are important evolutionary trajectories for the emergence of prosocial behavior in birds.

Our results reveal that cooperative breeding is positively associated with the propensity for prosocial behaviors in corvids, but that this main effect is qualified by an interaction with sex. Additional separate analyses for the two sexes showed that both cooperative breeding and colonial nesting positively affected prosociality, albeit differently for the two sexes. Consequently, our results support both the cooperative breeding hypothesis (Burkart et al., 2014; Burkart et al., 2009), which emphasizes the role of allomaternal care, and the self-domestication hypothesis (Hare et al., 2012; Hare, 2017; Wrangham, 2019), which stresses the importance of low levels of reactive aggression and high levels of social tolerance, as explanatory approaches for the evolution of prosocial behavior in the corvid family. An additional model that controlled for common ancestry confirmed the importance of both cooperative breeding and colonial nesting and showed that the phylogenetic signal was weak in terms of prosocial behaviors in corvids.

The conclusion that both cooperative breeding and colonial nesting positively affect prosocial behavior in corvids is corroborated by the species-specific provisioning rates in our study: provisioning was particularly high in the cooperatively breeding, colonially nesting azure-winged magpies (64–98%), high in the facultative cooperatively breeding, territorially nesting carrion crows (57%), and intermediate in the non-cooperatively breeding, colonially nesting jackdaws (33%). In the third colonial species, the rooks, very little food was provided during the prosocial test (2%). However, in this group only three out of 12 individuals could be habituated to the apparatus despite extensive training (see Appendix 1—table 1). Therefore, it is possible that the limited number of possible donors and recipients prevented higher provisioning rates. The provisioning results obtained in jackdaws parallel previous findings with this species when tested in a dyadic prosocial choice paradigm: in that study the jackdaws also provided food for their conspecifics in certain contexts (e.g. more provisioning for opposite-sex recipients; Schwab et al., 2012). Carrion crows, however, were previously not found to exhibit prosocial tendencies in a token exchange paradigm where they had the opportunity to transfer tokens to a conspecific partner, which could in turn be exchanged for food (Wascher et al., 2020). The authors of that study argued that the exchange paradigm might have been too complicated for the birds, as it required understanding the value of the tokens (Wascher et al., 2020). It is therefore possible that the GSP used in the current study, which simply required the birds to land on the provisioning perch in order to make food available for the group members, made it easier for the carrion crows to express their prosocial behavior.

An interesting exception to the predicted pattern is the remarkably high provisioning rate in one group of New Caledonian crows (70%). According to Cockburn, 2006, however, it remains unknown whether this species might engage in cooperative breeding. New Caledonian crows allow their offspring to stay in the parental territory for up to two consecutive breeding seasons (Holzhaider et al., 2011) and feed the juveniles for up to ten months post-fledging (Hunt et al., 2012). Helping by offspring at the nest has never been documented (Holzhaider et al., 2011), but it has proven difficult to observe interactions at the nest in most habitats. Family living, where offspring delay dispersal from the parental territory beyond nutritional independence, has been suggested as one of the evolutionary routes to cooperative breeding (Griesser et al., 2017; Brown, 1974). Nevertheless, Siberian jays, which also live in family groups (Griesser et al., 2017), showed no prosocial behavior in our study. However, one has to consider, that the Siberian jays were the only species not tested in captivity but in the wild. Although the study population is well habituated to the presence of humans and to field experiments (Griesser, 2013), it is possible that they were not as focused on the experiment as the captive species. Additionally, Siberian jays fully rely on scatter hoarding to survive the winters at the study site. Since this behavior has been shown to be predominantly selfish (Ekman et al., 1996), it is possible that Siberian jays’ particular feeding strategy explains their lack of prosocial tendencies. Therefore, to advance understanding of the role of family living in regard to prosociality, it would be important to further investigate prosocial tendencies in other family-living corvid species (Uomini et al., 2020).

In line with the original comparative study using the GSP in primates (Burkart et al., 2014), we corrected the percentage of provided food by including only provisioning by individuals that passed the criterion of landing significantly more often in the test compared to both control conditions, thereby giving the most conservative measure of prosocial provisioning. The rate of individuals that passed this criterion ranged from 0% to 50% across species (see Appendix 1—table 1 for details). Due to the experimental paradigm (i.e. the group setting) it is difficult to unequivocally conclude that the individuals that did not pass this criterion did not understand the task. These individuals might have been willing to land on the apparatus in the prosocial test, but might have simply been slower than other group members. Alternatively, they might have understood the difference between the prosocial test and the two control tasks, but they might just not have had prosocial tendencies. Given that explanation, it is interesting to note that the percentage of birds that passed the criterion was relatively high in the cooperatively breeding and/or colonial species (azure-winged magpies: 4 out of 8 birds (50%); carrion crows: 2 out of 6 (33%); Eurasian jackdaws: 2 out of 10 (20%); rooks: 1 out of 3 (33%)) and relatively lower in most territorial species (New Caledonian crows: 1 out of 5 (20%); common ravens: 1 out of 7 (14%); large-billed crows: 1 out of 9 (11%); Siberian jays: 0 out of 7 (0%)), especially as there is no reason to assume that the latter are cognitively less developed than the former (see e.g., Güntürkün and Bugnyar, 2016). When looking at the number of landings on the provisioning perch (i.e. with and without actual provisioning) of these 12 birds that passed the criterion, we only found a non-significant trend of more landings from the birds from colonial species than from the birds from territorial species and no effect of whether the birds came from a cooperatively breeding species or not. However, an individual would only pass this criterion if it landed relatively often on the provisioning perch in the prosocial test, thereby inherently also demonstrating a prosocial tendency (Burkart et al., 2014). Therefore, it is not surprising that among this group of birds, no strong differences according to cooperative breeding and colonial nesting became apparent with regard to prosocial tendencies. Additionally, the small sample size did not allow us to include further factors in the analysis (e.g. sex) and might have hampered the detection of potential differences.

Across all individuals we found that sex modulated the effects of both cooperative breeding and colonial nesting on how often the birds landed on the provisioning perch. The positive effect of cooperative breeding on the number of landings in the prosocial test was mainly driven by the females, although the results of the female-only model were not very robust. Nevertheless, the fact that the females from cooperatively breeding species were particularly prosocial is surprising, because observations in wild populations showed that in many cooperatively breeding corvids only a minority of the helpers were females (e.g. azure-winged magpies [Ren et al., 2016], their closely related sister species the Iberian magpies [Valencia et al., 2003], carrion crows [Baglione et al., 2002]) and that male helpers provided more care during breeding than females (e.g. carrion crows [Canestrari et al., 2005]). However, due to the high energetic demand of incubation that usually only the females incur, cooperatively breeding females might depend more on helpers’ contributions than males and they might use acts of prosocial behavior throughout the year (note that our studies were all conducted outside the breeding season) to incentivize group members to remain in the group. This argument is in line with the interdependence hypothesis, which states that cooperative acts are expected most when individuals strongly rely on each other (Roberts, 2005). In contrast, among colonially nesting birds, male individuals, but not females, were particularly prosocial, together with an overall main effect of stronger prosocial tendencies in males than in females across all tested groups. According to costly signaling theory (Zahavi, 1997), prosocial acts can be regarded as honest signals that advertise the donor’s underlying qualities (e.g. health, strength, ability to control resources; cf. competitive altruism hypothesis; Hardy and Van Vugt, 2006). Based on these premises, dominant individuals would be expected to show more prosocial behavior than subordinates. This prediction has been supported by experimental evidence from birds (Duque and Stevens, 2016) and several primate species (e.g. long-tailed macaques; Massen et al., 2010; for a review, see Marshall-Pescini et al., 2016). In most corvids, males are dominant over females (Scheid et al., 2008; Massen et al., 2014; Wechsler, 1988; Ode et al., 2015; Chiarati et al., 2010; Sklepkovych, 1997) and would therefore be expected to face greater pressure to advertise their dominance rank than females. This might be most evident in colonial males, which nest in close proximity with many conspecifics and consequently engaging in dominance challenges might be particularly costly for them (Verhulst and Salomons, 2004). The self-domestication hypothesis also emphasizes the importance of reduced reactive aggression and violent conflict between male individuals, not females, as an important factor for the evolution of human-like prosociality (Wrangham, 2019). Beyond that, prosocial actions might represent an attempt of males to trade food for extra-pair copulations (Tryjanowski and Hromada, 2005) or to maintain relationships with affiliative partners other than the mated partner (Miyazawa et al., 2020; von Bayern et al., 2007; Boucherie et al., 2016). In general, the results from the single sex models – especially the female-only model – have to be considered preliminary due to the low sample size. Future studies with larger sample sizes and experiments that specifically address these sex differences are needed to reveal which of these hypotheses explain the sex-specific effects of both cooperative and colonial breeding in birds.

One additional limitation of this study was that, despite the considerable research effort of this multi-lab study, we only managed to test few replicates per species. Finding test populations is a common problem for large-scale comparative studies (e.g. the original GSP study in primates [Burkart et al., 2014]; see also Morales Picard et al., 2020; O'Hara et al., 2017; MacLean et al., 2014; Many Primates et al., 2019). While the provisioning rates were similar in the two groups of azure-winged magpies (i.e. the two highest provisioning rates at 98% and 64%, respectively) and the two groups of Siberian jays (i.e. both 0%), there was a substantial difference between the two groups of New-Caledonian crows: in one group, 70% of the available food was provided to the group members, whereas in the other group there was no successful provisioning at all. One has to consider, though, that the latter group consisted only of two individuals at the time of testing. Therefore, similarly as in the rooks, the limited number of potential donors and recipients might have prevented successful provisioning. Also, within the groups, there was obvious inter-individual variation, with some individuals providing the majority of the food to their group members while other individuals rarely landed on the provisioning perch at all. Due to the unrestricted group setting of the GSP, it is not possible to discern whether the individuals that did not land on the provisioning perch were not motivated to provide food for their group members, or whether they were merely too slow to do so compared to other individuals that for example were bolder or faster. To be able to more confidently demonstrate true species generalizations and rule out a strong effect of individual characteristics, future studies should attempt to increase the number of replicates per species and should bolster the results of the GSP with individual testing paradigms (e.g. prosocial choice experiments).

Within the groups, we would have expected more opposite-sex provisioning than same-sex provisioning, especially from males to females. Observations of naturally occurring food sharing suggest that food provisioning in corvids might serve the function of forming pair bonds and social bonds in general (Massen et al., 2015a; Miyazawa et al., 2020; von Bayern et al., 2007). Also in the context of a prosocial choice experiment with jackdaws, opposite-sex recipients were more likely to elicit prosocial behavior from the donors than same-sex recipients (Schwab et al., 2012). Similarly, in an active food-sharing paradigm, azure-winged magpies shared high-value food items preferably with, although not restricted to, members of the opposite sex (Massen et al., 2020). However, both opposite-sex and same-sex provisioning occurred equally often in our study. This might have been because of the constraints of the GSP, where food is made available to the whole group and the donor has limited possibilities to influence the specific recipient of its prosocial action. There were some differences in the distribution of donor-recipient sex-constellations, which could, however, not be linked back to either cooperative breeding or nesting type, but were more likely a result of the specific group compositions. Interestingly, although the majority of the tested birds were adults, many instances of juveniles providing food to adults were observed in both the azure-winged magpies and the New Caledonian crows, which accounted for almost all the provided food in the latter species. Prosocial acts from juveniles are expected in cooperatively breeding species based on observations in the wild (e.g. Iberian magpies [Valencia et al., 2003]; carrion crows [Baglione et al., 2002]). In contrast, New Caledonian crow parents feed their juvenile offspring for extended periods (Hunt et al., 2012), while food provisioning by juveniles has never been documented (Holzhaider et al., 2011). Our finding of prosocial behavior in a juvenile New Caledonian crow underlines the importance of considering the role of family living in the absence of cooperative breeding for the evolution of prosociality in birds (Uomini et al., 2020). Future studies, where samples show larger age variation within the groups or where the same groups can be tested at different time points with differing age ratios, would also be very informative regarding the question of the influence of age on prosocial behavior (Kaplan, 2020). An additional factor that has been argued to play an important role for prosocial acts between individuals is their relatedness (e.g. Bourke, 2014; but see Schweinfurth and Taborsky, 2018b). However, since kinship relations between individuals were unknown for about half of the groups tested in the current study, we were not able to include kinship as a factor in the analysis. Future studies that track relatedness between group members could further investigate the relevance of this factor for prosocial behavior in corvids.

In contrast to the comparative study on primate prosociality (Burkart et al., 2014), we did not use the degree of allomaternal care, but rather a nominal classification as either cooperatively breeding species or not as a predictor in our models. The reasoning for that change was two-fold. First, there is less information on the specific number and degree of investment of helpers in cooperatively breeding bird species (Cockburn, 2006) compared to primates (Isler and van Schaik, 2012) and even within the same corvid species, the numbers seem to differ greatly depending on the population (e.g. Komeda et al., 1987; Ren et al., 2016; Valencia et al., 2003; Baglione et al., 2002). Second, since we only had two cooperatively breeding species in our sample, a more detailed representation of the degree of cooperative breeding would have decreased the statistical power of our analysis. Additionally, it is important to note that – differently from the general trend in primates – all the species included in our sample express bi-parental care (i.e. care provided by the father and the mother), meaning that there is a certain degree of allomaternal care even in non-cooperatively breeding, territorial corvid species. Future studies that more elaborately evaluate the degree of allomaternal care in wild corvid populations are thus needed to create a comprehensive comparison between the corvids in this study and the primates (Burkart et al., 2014).

The evenness of access to food was medium to high in all tested species in our study (Burkart et al., 2014). Following the argument of the original study in primates (Burkart et al., 2014), that would indicate medium-to-high levels of social tolerance in all groups, irrespective of the prevalence of cooperative breeding or colonial nesting. However, the relatively even access to food among the group members may reflect that most corvids have a tendency to cache food for later consumption (de Kort and Clayton, 2006). In our study, even the most dominant birds rarely monopolized the apparatus for long durations, as it has been documented in despotic primate species (Schnoell and Kappeler, 2018). The corvids rather periodically left the area to cache their obtained food out of sight of their conspecifics (Bugnyar et al., 2016). Therefore, the evenness of access to food in phase II of the GSP might not be a valid proxy for social tolerance in corvids. Other approaches like co-feeding experiments might provide more suitable measures of social tolerance, because they measure how tolerant the individuals of a given group or species are to foraging in close proximity with other group members (Sima et al., 2016). Nevertheless, the use of the GSP has many advantages when attempting to conduct a comprehensive experimental investigation of prosocial behavior (Burkart et al., 2014): the apparatus and procedure are cognitively not demanding and testing individuals within their social groups and home environment reduces stress and increases animal welfare. Additionally, the paradigm offers several criteria to assess whether an individually was sufficiently habituated/trained and its propensity to land on the apparatus was not caused by a lack of inhibitory control. Overall, the birds tested in this study differentiated between the prosocial test and both control conditions and landed more often on the provisioning perch when they could provide food to their group members than when there was no food or when access to the food was blocked for the recipient (see Appendix 1—figure 1). Therefore, the GSP is a highly useful paradigm for comparative investigations of animal prosociality and can be conceivable applied to a much wider range of species and taxa.

The current study is a first attempt to determine how generalizable the predictions of the cooperative breeding hypothesis and self-domestication hypothesis are, or whether they are actually restricted to the primate order (Thornton and McAuliffe, 2015). In a systematic comparison of prosocial preferences across eight corvid species we find, in fact, evidence for both hypotheses. It is important to note, however, that these two hypotheses are not mutually exclusive and that one common underlying mechanism in both hypotheses is likely a heightened level of social tolerance at the nest. In cooperatively breeding species, helpers have to show increased social tolerance toward offspring that is not their own, while the breeders have to tolerate older offspring and immigrant helpers in their territories and close to their nests. In colonially nesting species, a breeding pair has to tolerate the proximity of other breeding pairs close to their nest. Consequently, the combined results of our study strongly suggest that both cooperative breeding and the heightened social tolerance required by colonial nesting are likely evolutionary pathways to prosocial behavior in corvids.

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Author details

1. Lisa Horn

   Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria

   Contribution

   Conceptualization, Data curation, Formal analysis, Supervision, Validation, Investigation, Visualization, Methodology, Writing - original draft, Project administration, Writing - review and editing

   For correspondence

   lisa.horn@univie.ac.at

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9586-915X

2. Thomas Bugnyar

   Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria

   Contribution

   Conceptualization, Supervision, Funding acquisition, Methodology, Writing - review and editing

   Competing interests

   No competing interests declared

3. Michael Griesser

   1. Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland
   2. Department of Biology, University of Konstanz, Konstanz, Germany
   3. Center for the Advanced Study of Collective Behaviour, University of Konstanz, Konstanz, Germany

   Contribution

   Formal analysis, Funding acquisition, Writing - review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-2220-2637

4. Marietta Hengl

   1. Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
   2. Eulen- und Greifvogelstation Haringsee, Haringsee, Austria

   Contribution

   Data curation, Funding acquisition, Investigation

   Competing interests

   No competing interests declared

5. Ei-Ichi Izawa

   Department of Psychology, Keio University, Tokyo, Japan

   Contribution

   Data curation, Funding acquisition, Investigation, Writing - review and editing

   Competing interests

   No competing interests declared

6. Tim Oortwijn

   Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland

   Contribution

   Data curation, Investigation, Writing - review and editing

   Competing interests

   No competing interests declared

7. Christiane Rössler

   Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria

   Contribution

   Data curation, Funding acquisition, Investigation, Writing - review and editing

   Competing interests

   No competing interests declared

8. Clara Scheer

   1. Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
   2. Faculty of Psychology, Education and Sports, University of Regensburg, Regensburg, Germany

   Contribution

   Conceptualization, Data curation, Investigation, Methodology

   Competing interests

   No competing interests declared

9. Martina Schiestl

   Department of Linguistic and Cultural Evolution, Max Planck Institute for the Science of Human History, Jena, Germany

   Contribution

   Data curation, Investigation

   Competing interests

   No competing interests declared

10. Masaki Suyama

    Department of Behavioral Sciences, Hokkaido University, Sapporo, Japan

    Contribution

    Data curation, Funding acquisition, Investigation

    Competing interests

    No competing interests declared

11. Alex H Taylor

    School of Psychology, University of Auckland, Auckland, New Zealand

    Contribution

    Funding acquisition, Writing - review and editing

    Competing interests

    No competing interests declared

12. Lisa-Claire Vanhooland

    Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria

    Contribution

    Funding acquisition, Validation, Investigation

    Competing interests

    No competing interests declared

13. Auguste MP von Bayern

    Max-Planck-Institute for Ornithology, Seewiesen, Germany

    Contribution

    Funding acquisition, Writing - review and editing

    Competing interests

    No competing interests declared

14. Yvonne Zürcher

    Department of Anthropology, University of Zurich, Zurich, Switzerland

    Contribution

    Data curation, Investigation

    Competing interests

    No competing interests declared

15. Jorg JM Massen

    1. Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
    2. Animal Ecology Group, Department of Biology, Utrecht University, Utrecht, Netherlands

    Contribution

    Conceptualization, Supervision, Funding acquisition, Methodology, Writing - review and editing

    Competing interests

    No competing interests declared

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