Jennifer K. Hellmann

Reproductive sharing in relation to group and colony-level attributes in a cooperative breeding fish

The degree to which group members share reproduction is dictated by both within-group (e.g. group size and composition) and between-group (e.g. density and position of neighbours) characteristics. While many studies have investigated reproductive patterns within social groups, few have simultaneously explored how within-group and between-group social structure influence these patterns. Here, we investigated how group size and composition, along with territory density and location within the colony, influenced parentage in 36 wild groups of a colonial, cooperatively breeding fish Neolamprologus pulcher. Dominant males sired 76% of offspring in their group, whereas dominant females mothered 82% of offspring in their group. Subordinate reproduction was frequent, occurring in 47% of sampled groups. Subordinate males gained more paternity in groups located in high-density areas and in groups with many subordinate males. Dominant males and females in large groups and in groups with many reproductively mature subordinates had higher rates of parentage loss, but only at the colony edge. Our study provides, to our knowledge, the first comprehensive quantification of reproductive sharing among groups of wild N. pulcher, a model species for the study of cooperation and social behaviour. Further, we demonstrate that the frequency of extra-pair parentage differs across small social and spatial scales.

Within-group relatedness is correlated with colony-level social structure and reproductive sharing in a social fish

In group‐living species, the degree of relatedness among group members often governs the extent of reproductive sharing, cooperation and conflict within a group. Kinship among group members can be shaped by the presence and location of neighbouring groups, as these provide dispersal or mating opportunities that can dilute kinship among current group members. Here, we assessed how within‐group relatedness varies with the density and position of neighbouring social groups in Neolamprologus pulcher, a colonial and group‐living cichlid fish. We used restriction site‐associated DNA sequencing (RADseq) methods to generate thousands of polymorphic SNPs. Relative to microsatellite data, RADseq data provided much tighter confidence intervals around our relatedness estimates. These data allowed us to document novel patterns of relatedness in relation to colony‐level social structure. First, the density of neighbouring groups was negatively correlated with relatedness between subordinates and dominant females within a group, but no such patterns were observed between subordinates and dominant males. Second, subordinates at the colony edge were less related to dominant males in their group than subordinates in the colony centre, suggesting a shorter breeding tenure for dominant males at the colony edge. Finally, subordinates who were closely related to their same‐sex dominant were more likely to reproduce, supporting some restraint models of reproductive skew. Collectively, these results demonstrate that within‐group relatedness is influenced by the broader social context, and variation between groups in the degree of relatedness between dominants and subordinates can be explained by both patterns of reproductive sharing and the nature of the social landscape.

Sex and social status affect territorial defence in a cooperatively breeding cichlid fish, Neolamprologus savoryi

Members of social groups must defend their shared territory against both predators and competitors. However, individuals differ widely in their contributions to territorial defence. Assessing the variation in response to territorial intrusions provides insight into both the benefits and costs of group living for different group members. In this study, we assessed the response of wild Neolamprologus savoryi to experimentally staged territorial intrusions. Neolamprologus savoryi is an understudied cooperatively breeding cichlid fish endemic to Lake Tanganyika, East Africa. We found that dominant male and dominant female N. savoryi were both highly aggressive towards heterospecific predators and towards same-sex conspecific rivals. Both dominant males and females were less aggressive towards opposite-sex conspecific opponents, with the relative reduction in aggression being most pronounced in males. Subordinates provided low levels of defence against all intruder types, which suggests that subordinate N. savoryi rely on larger group members for protection. Collectively, our results provide insight into the structure and function of N. savoryi social groups, and highlights key costs and benefits of cooperation for individual social group members.

Variation in glucocorticoid levels in relation to direct and third-party interactions in a social cichlid fish

In complex animal societies, direct interactions between group members can influence the behavior and glucocorticoid levels of individuals involved. Recently, it has become apparent that third-party group members can influence dyadic interactions, and vice versa. Thus, glucocorticoid levels may vary depending on interactions of other members of the social group. Using the social cichlid fish Neolamprologus pulcher, we examined the relationship between levels of the glucocorticoid hormone cortisol in subordinate females and 1) direct interactions with dominant group members, as well as 2) dyadic interactions between the dominant male and female, in which the subordinate female was not directly involved. Subordinate females that frequently engaged in non-aggressive interactions with dominant females had lower cortisol levels. There was no relationship between subordinate female cortisol and agonistic interactions between the subordinate female and either dominant. Subordinate females had higher cortisol levels when in groups in which the dominant breeding pair behaved agonistically towards each other and performed fewer courtship behaviors. For subordinate females in this species, variation in cortisol levels is associated with their own affiliative behavior, but also can be explained by the broader social context of interactions between dominant members of the group.

Social status influences responses to unfamiliar conspecifics in a cooperatively breeding fish

In group living animals, individuals may visit other groups. The costs and benefits of such visits for the members of a group will depend on the attributes and intentions of the visitor, and the social status of responding group members. Using wild groups of the cooperatively breeding cichlid fish ( Neolamprologus pulcher ), we compared group member responses to unfamiliar ‘visiting’ conspecifics in control groups and in experimentally manipulated groups from which a subordinate the same size and sex as the visitor was removed. High-ranking fish were less aggressive towards visitors in removal groups than in control groups; low-ranking subordinates were more aggressive in the removal treatment. High-ranking females and subordinates the same size and sex as the visitor responded most aggressively toward the visitor in control groups. These results suggest that visitors are perceived as potential group joiners, and that such visits impose different costs and benefits on current group members.

Intragroup social dynamics vary with the presence of neighbors in a cooperatively breeding fish

Abstract Conflict is an inherent part of social life in group-living species. Group members may mediate conflict through submissive and affiliative behaviors, which can reduce aggression, stabilize dominance hierarchies, and foster group cohesion. The frequency and resolution of within-group conflict may vary with the presence of neighboring groups. Neighbors can threaten the territory or resources of the whole group, promoting behaviors that foster within-group cohesion. However, neighbors may also foster conflict of interests among group members: opportunities for subordinate dispersal may alter conflict among dominants and subordinates while opportunities for extra-pair reproduction may increase conflict between mates. To understand how neighbors mediate within-group conflict in the cooperatively breeding fish Neolamprologus pulcher, we measured behavioral dynamics and social network structure in isolated groups, groups recently exposed to neighbors, and groups with established neighbors. Aggression and submission between the dominant male and female pair were high in isolated groups, but dominant aggression was directly primarily at subordinates when groups had neighbors. This suggests that neighbors attenuate conflict between mates and foster conflict between dominants and subordinates. Further, aggression and submission between similarly sized group members were most frequent when groups had neighbors, suggesting that neighbors induce rank-related conflict. We found relatively little change in within-group affiliative networks across treatments, suggesting that the presence of neighbors does not alter behaviors associated with promoting group cohesion. Collectively, these results provide some of the first empirical insights into the extent to which intragroup behavioral networks are mediated by intergroup interactions and the broader social context.

Dominant and subordinate outside options alter help and eviction in a pay-to-stay negotiation model

Subordinates “pay rent” to stay in their group, but pay less when they can move elsewhere. For many animals, group living comes with costs: smaller individuals get evicted unless they help on the territory. Using theoretical models, we show that negotiation is key to enforcing pay-to-stay cooperation: subordinates provide fitness benefits to dominants and negotiate help based on breeding opportunities outside the group, but only when subordinates can plastically increase help in response to demanding dominants.

Isotocin neuronal phenotypes differ among social systems in cichlid fishes

Social living has evolved numerous times across a diverse array of animal taxa. An open question is how the transition to a social lifestyle has shaped, and been shaped by, the underlying neurohormonal machinery of social behaviour. The nonapeptide neurohormones, implicated in the regulation of social behaviours, are prime candidates for the neuroendocrine substrates of social evolution. Here, we examined the brains of eight cichlid fish species with divergent social systems, comparing the number and size of preoptic neurons that express the nonapeptides isotocin and vasotocin. While controlling for the influence of phylogeny and body size, we found that the highly social cooperatively breeding species (n = 4) had fewer parvocellular isotocin neurons than the less social independently breeding species (n = 4), suggesting that the evolutionary transition to group living and cooperative breeding was associated with a reduction in the number of these neurons. In a complementary analysis, we found that the size and number of isotocin neurons significantly differentiated the cooperatively breeding from the independently breeding species. Our results suggest that isotocin is related to sociality in cichlids and may provide a mechanistic substrate for the evolution of sociality.

A comparative study of an innate immune response in Lamprologine cichlid fishes.

Social interactions facilitate pathogen transmission and increase virulence. Therefore, species that live in social groups are predicted to suffer a higher pathogen burden, to invest more heavily in immune defence against pathogens, or both. However, there are few empirical tests of whether social species indeed invest more heavily in immune defence than non-social species. In the current study, we conducted a phylogenetically controlled comparison of innate immune response in Lamprologine cichlid fishes. We focused on three species of highly social cichlids that live in permanent groups and exhibit cooperative breeding (Julidochromis ornatus, Neolamprologus pulcher and Neolamprologus savoryi) and three species of non-social cichlids that exhibit neither grouping nor cooperative behaviour (Telmatochromis temporalis, Neolamprologus tetracanthus and Neolamprologus modestus). We quantified the innate immune response by injecting wild fishes with phytohaemagglutinin (PHA), a lectin that causes a cell-mediated immune response. We predicted that the three highly social species would show a greater immune reaction to the PHA treatment, indicating higher investment in immune defence against parasites relative to the three non-social species. We found significant species-level variation in immune response, but contrary to our prediction, this variation did not correspond to social system. However, we found that immune response was correlated with territory size across the six species. Our results indicate that the common assumption of a positive relationship between social system and investment in immune function may be overly simplistic. We suggest that factors such as rates of both in-group and out-group social interactions are likely to be important mediators of the relationship between sociality and immune function.