Social experience in early ontogeny has lasting effects on social skills in cooperatively breeding cichlids

The early social environment can affect the social behaviour of animals throughout life. We tested whether the presence of adults during early development influences the social behaviour of juveniles later on in the cooperatively breeding cichlid 'Neolamprologus pulcher'. In a split-brood design we raised half of the broods together with parents and with or without brood care helpers, and the other half without adults. During early rearing, fry raised with adults showed more aggressive and submissive behaviour to each other than fish raised with siblings only. After transferring the young to a neutral environment lacking adult conspecifics we tested their social performance in a competitive situation. Either young were assigned the ownership of a shelter or they had no shelter of their own. As shelter owners, fish that had been raised with adults showed more of an energetically cheaper, restrained form of aggression, while as intruders they behaved submissively more often than fish raised without adults. The strength of these treatment effects depended on the opponent's social experience, and contests were terminated earlier only when both opponents had been raised with adults. Our results show that the social-rearing conditions persistently affect the economy and adequacy of individual reactions to social challenges, which is reminiscent of social competence effects known from humans. Remarkably, during the social treatment period brood care involved only protection but no direct interactions between adults and young. We discuss potential mechanisms by which the presence of brood-caring adults may persistently affect social skills in animals

Unexpected patterns of plastic energy allocation in stochastic environments

When environmental conditions vary stochastically, individuals accrue fitness benefits by exhibiting phenotypic plasticity. Such benefits may be counterbalanced by costs of plasticity that increase with the exhibited degree of plasticity. Here we introduce and analyze a general dynamic- programming model describing an individuals optimal energy allocation in a stochastic environment. After maturation, individuals decide repeatedly how to allocate incoming energy between reproduction and maintenance. We investigate the optimal fraction of energy invested into reproduction and the resultant degree of plasticity in dependence on the variability and predictability of the environment. Our analyses reveal unexpected patterns of optimal energy allocation. In environments with very low energy availability, all energy is allocated to reproduction, although this implies that individuals will not survive after reproduction. Above a certain threshold of energy availability, the optimal reproductive investment rapidly decreases to a minimum, and even vanishes entirely when the environment is highly variable. With further improvement of energy availability, optimal reproductive investment gradually increases again, until almost all energy is allocated to reproduction. Costs of plasticity affect this allocation pattern only quantitatively. Our results show that optimal reproductive investment does not increase monotonically with growing energy availability and that small changes in energy availability can lead to major variations in optimal energy allocation. Our results help to unify two apparently opposing predictions from life-history theory, that organisms should increase reproductive investment both with improved environmental conditions and when conditions deteriorate ('terminal investment')

Life-stage specific environments in a cichlid fish: Implications for inducible maternal effects

Through environmentally induced maternal effects females may fine-tune their offspring's phenotype to the conditions offspring will encounter after birth. If juvenile and adult ecologies differ, the conditions that mothers experienced as juveniles may better predict their offspring's environment than the adult females' ambient conditions. Maternal effects induced by the environment experienced by females during their early ontogeny should evolve when three ecological conditions are met: (i) Adult ecology does not predict the postnatal environmental conditions of offspring; (ii) Environmental conditions for juveniles are correlated across successive generations; and (iii) Juveniles occasionally settle in conditions that differ from the juvenile habitat of their mothers. By combining size-structured population counts, ecological surveys and a genetic analysis of population structure we provide evidence that all three conditions hold for Simochromis pleurospilus, a cichlid fish in which mothers adjust offspring quality to their own juvenile ecology. Adults of many species cannot predict offspring's environment from ambient cues. Hence we predict that life-stage specific maternal effects are common in animals. Therefore, it is important to incorporate parental ontogeny in the study of parental effects when juveniles and adults inhabit different environments

Consistent cooperation in a cichlid fish is caused by maternal and developmental effects rather than heritable genetic variation.

This is the author accepted manuscript. The final version is available from Royal Society via the DOI in this record.Studies on the evolution of cooperative behaviour are typically confined to understanding its adaptive value. It is equally essential, however, to understand its potential to evolve, requiring knowledge about the phenotypic consistency and genetic basis of cooperative behaviour. While previous observational studies reported considerably high heritabilities of helping behaviour in cooperatively breeding vertebrates, experimental studies disentangling the relevant genetic and non-genetic components of cooperative behaviour are lacking. In a half-sibling breeding experiment, we investigated the repeatability and heritability of three major helping behaviours performed by subordinates of the cooperatively breeding fishNeolamprologus pulcherTo experimentally manipulate the amount of help needed in a territory, we raised the fish in two environments differing in egg predation risk. All three helping behaviours were significantly repeatable, but had very low heritabilities. The high within-individual consistencies were predominantly due to maternal and permanent environment effects. The perceived egg predation risk had no effect on helping, but social interactions significantly influenced helping propensities. Our results reveal that developmentally plastic adjustments of provided help to social context shape cooperative phenotypes, whereas heritable genetic variation plays a minor role.Funding was provided by the ‘ProDoc’ program of the Swiss National Science Foundation (SNF, projects PDFMP3_137196 and 31003A_156881 to B.T.), and the ‘120% support grant’ to C.K. of the University of Bern

Predator-induced maternal effects determine adaptive antipredator behaviors via egg composition.

In high-risk environments with frequent predator encounters, efficient antipredator behavior is key to survival. Parental effects are a powerful mechanism to prepare offspring for coping with such environments, yet clear evidence for adaptive parental effects on offspring antipredator behaviors is missing. Rapid escape reflexes, or "C-start reflexes," are a key adaptation in fish and amphibians to escape predator strikes. We hypothesized that mothers living in high-risk environments might induce faster C-start reflexes in offspring by modifying egg composition. Here, we show that offspring of the cichlid fish Neolamprologus pulcher developed faster C-start reflexes and were more risk averse if their parents had been exposed to cues of their most dangerous natural predator during egg production. This effect was mediated by differences in egg composition. Eggs of predator-exposed mothers were heavier with higher net protein content, and the resulting offspring were heavier and had lower igf-1 gene expression than control offspring shortly after hatching. Thus, changes in egg composition can relay multiple putative pathways by which mothers can influence adaptive antipredator behaviors such as faster escape reflexes

Environmental Change Enhances Cognitive Abilities in Fish

Cichlid fish subjected to a single change in food ration early in life show enhanced learning abilities during juvenile and adult stages

Paternity of Subordinates Raises Cooperative Effort in Cichlids

Background In cooperative breeders, subordinates generally help a dominant breeding pair to raise offspring. Parentage studies have shown that in several species subordinates can participate in reproduction. This suggests an important role of direct fitness benefits for cooperation, particularly where groups contain unrelated subordinates. In this situation parentage should influence levels of cooperation. Here we combine parentage analyses and detailed behavioural observations in the field to study whether in the highly social cichlid Neolamprologus pulcher subordinates participate in reproduction and if so, whether and how this affects their cooperative care, controlling for the effect of kinship. Methodology/Principal Findings We show that: (i) male subordinates gained paternity in 27.8% of all clutches and (ii) if they participated in reproduction, they sired on average 11.8% of young. Subordinate males sharing in reproduction showed more defence against experimentally presented egg predators compared to subordinates not participating in reproduction, and they tended to stay closer to the breeding shelter. No effects of relatedness between subordinates and dominants (to mid-parent, dominant female or dominant male) were detected on parentage and on helping behaviour. Conclusions/Significance This is the first evidence in a cooperatively breeding fish species that the helping effort of male subordinates may depend on obtained paternity, which stresses the need to consider direct fitness benefits in evolutionary studies of helping behaviour

An evolutionary perspective on stress responses, damage and repair

This is the final version. Available on open access from Elsevier via the DOI in this record. Variation in stress responses has been investigated in relation to environmental factors, species ecology, life history and fitness. Moreover, mechanistic studies have unravelled molecular mechanisms of how acute and chronic stress responses cause physiological impacts (‘damage’), and how this damage can be repaired. However, it is not yet understood how the fitness effects of damage and repair influence stress response evolution. Here we study the evolution of hormone levels as a function of stressor occurrence, damage and the efficiency of repair. We hypothesise that the evolution of stress responses depends on the fitness consequences of damage and the ability to repair that damage. To obtain some general insights, we model a simplified scenario in which an organism repeatedly encounters a stressor with a certain frequency and predictability (temporal autocorrelation). The organism can defend itself by mounting a stress response (elevated hormone level), but this causes damage that takes time to repair. We identify optimal strategies in this scenario and then investigate how those strategies respond to acute and chronic exposures to the stressor. We find that for higher repair rates, baseline and peak hormone levels are higher. This typically means that the organism experiences higher levels of damage, which it can afford because that damage is repaired more quickly, but for very high repair rates the damage does not build up. With increasing predictability of the stressor, stress responses are sustained for longer, because the animal expects the stressor to persist, and thus damage builds up. This can result in very high (and potentially fatal) levels of damage when organisms are exposed to chronic stressors to which they are not evolutionarily adapted. Overall, our results highlight that at least three factors need to be considered jointly to advance our understanding of how stress physiology has evolved: (i) temporal dynamics of stressor occurrence; (ii) relative mortality risk imposed by the stressor itself versus damage caused by the stress response; and (iii) the efficiency of repair mechanisms.Swiss National Science FoundationRoyal SocietyAcademy of FinlandSwedish Research Counci

Towards an evolutionary theory of stress responses

This is the author accepted manuscript. The final version is available from Elsevier via the DOI in this recordAll organisms have a stress response system to cope with environmental threats, yet its precise form varies hugely within and across individuals, populations and species. While the physiological mechanisms are increasingly understood, how stress responses have evolved remains elusive. Here, we show that important insights can be gained from models that incorporate physiological mechanisms within an evolutionary optimality analysis (the ‘evo-mecho’ approach). Our approach reveals environmental predictability and physiological constraints as key factors shaping stress response evolution, generating testable predictions about variation across species and contexts. We call for an integrated research programme combining theory, experimental evolution and comparative analysis to advance scientific understanding of how this core physiological system has evolved.Conference Universitaire de Suisse Occidentale (CUSO)Swiss National Science FoundationUniversity of BristolRoyal SocietyAcademy of FinlandSwedish Research Counci