Predation risk is a major ecological factor selecting for group living. It is largely ignored, however, as an evolutionary driver of social complexity and cooperative breeding, which is attributed mainly to a combination of habitat saturation and enhanced relatedness levels. Social cichlids neither suffer from habitat saturation, nor are their groups composed primarily of relatives. This demands alternative ecological explanations for the evolution of advanced social organization. To address this question, we compared the ecology of eight populations of Neolamprologus pulcher, a cichlid fish arguably representing the pinnacle of social evolution in poikilothermic vertebrates. Results show that variation in social organization and behavior of these fish is primarily explained by predation risk and related ecological factors. Remarkably, ecology affects group structure more strongly than group size, with predation inversely affecting small and large group members. High predation and shelter limitation leads to groups containing few small but many large members, which is an effect enhanced at low population densities. Apparently, enhanced safety from predators by cooperative defense and shelter construction are the primary benefits of sociality. This finding suggests that predation risk can be fundamental for the transition toward complex social organization, which is generally undervalued. social evolution | social complexity | predation risk | ecological constraints | cooperative breeding

Summary1. Many anti-predator benefits of group living are predicted to scale with prey density. Nevertheless, evidence for a general density-dependent increase of prey survival is scarce. A possible reason for this discrepancy is the reduction of costly anti-predator behaviour of prey with increasing density, which may offset density-dependent survival gains. Benefits of group living might hence accrue by saved investment into anti-predator behaviours rather than by increased survival rates. 2. Here, we experimentally presented predators in a colony of the cooperatively breeding cichlid fish Neolamprologus pulcher to study density dependence of their anti-predator defences. Predation is a driver of the formation and stability of breeding groups in this species, but potential benefits of coloniality are yet unclear. We hypothesised that increased density of breeding groups would either increase total anti-predator behaviour or allow individuals to reduce their anti-predator effort due to enhanced predator deterrence from neighbours. 3. Confirming predictions from the second hypothesis, our results show that focal groups invested less into anti-predator behaviour at higher densities, while neighbouring groups' behaviour compensated for this reduced effort. This resulted in stable levels of anti-predator behaviours over the entire range of natural densities. Thus, aggregating in colonies allows these fish to save investment in anti-predator behaviour. 4. These results suggest that the formation of both breeding groups and colonies reflects adaptive responses to high predation pressure in this species. Two different levels of sociality seem to be favoured by the same selective force. 5. Our study provides experimental evidence in nature for an important benefit of coloniality that may explain the concomitant existence of different levels of sociality in many highly social taxa.

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Helping behaviour in cooperative breeders has been intensively studied in many animal taxa, including arthropods, birds and mammals. In these highly social systems, helpers typically engage in brood care and the protection of dependent young. Such helping systems also exist in cooperatively breeding cichlid species of Lake Tanganyika. However, breeding in these species happens in clefts, narrow holes or shelters underneath stones. Therefore, direct brood care by breeders and helpers has thus far only been observed under artificial laboratory conditions. Under natural conditions, brood care behaviour has been estimated indirectly by determining the time spent in the breeding chamber, or by the number of visits to the breeding chamber. The reliability of such substitutes needs to be validated, for instance, by demonstrating alloparental egg care of helpers through direct observations in nature. Here, we describe direct egg care by a male helper of the cooperatively breeding cichlid Neolamprologus savoryi in the field. The helper inspected and cleaned the eggs and defended them against predators. By reconstructing the genetic relatedness using microsatellite markers, we show that the helper was the son of the breeding male, but unrelated to the breeding female. The genetic mother of the helper was defending a different territory next to the one where the helper showed alloparental egg care. This indicates that the helper had dispersed inside the male territory to assist another female to care for his half‐siblings. These results demonstrate alloparental egg care without reproductive share in a fish species under natural conditions, underlining that helping behaviour in cooperatively breeding fish has a strong non‐self‐serving component.

Kin selection plays a major role in the evolution of cooperative systems. However, many social species exhibit complex withingroup relatedness structures, where kin selection alone cannot explain the occurrence of cooperative behavior. Understanding such social structures is crucial to elucidate the evolution and maintenance of multi-layered cooperative societies. In lamprologine cichlids, intragroup relatedness seems to correlate positively with reproductive skew, suggesting that in this clade dominants tend to provide reproductive concessions to unrelated subordinates to secure their participation in brood care. We investigate how patterns of within-group relatedness covary with direct and indirect fitness benefits of cooperation in a highly social vertebrate, the cooperatively breeding, polygynous lamprologine cichlid Neolamprologus savoryi. Behavioral and genetic data from 43 groups containing 578 individuals show that groups are socially and genetically structured into subgroups. About 17% of group members were unrelated immigrants, and average relatedness between breeders and brood care helpers declined with helper age due to group membership dynamics. Hence the relative importance of direct and indirect fitness benefits of cooperation depends on helper age. Our findings highlight how both direct and indirect fitness benefits of cooperation and group membership can select for cooperative behavior in societies comprising complex social and relatedness structures.