Divergence of developmental trajectories is triggered interactively by early social and ecological experience in a cooperative breeder

Abstract

Cooperative breeders feature the highest level of social complexity among vertebrates. Environmental constraints foster the evolution of this form of social organization, selecting for both well-developed social and ecological competences. Cooperative breeders pursue one of two alternative social trajectories: delaying reproduction to care for the offspring of dominant breeders or dispersing early to breed independently. It is yet unclear which ecological and social triggers determine the choice between these alternatives and whether diverging developmental trajectories exist in cooperative vertebrates predisposing them to dispersal or philopatry. Here we experimentally reared juveniles of cooperatively breeding cichlid fish by varying the social environment and simulated predation threat in a two-by-two factorial long-term experiment. First, we show that individuals develop specialized behavioral competences, originating already in the early postnatal phase. Second, these specializations predisposed individuals to pursue different developmental trajectories and either to disperse early or to extend philopatry in adulthood. Thus, our results contrast with the proposition that social specializations in early ontogeny should be restricted to eusocial species. Importantly, social and ecological triggers were both required for the generation of divergent life histories. Our results thus confirm recent predictions from theoretical models that organisms should combine relevant information from different environmental cues to develop integrated phenotypes.

Transcriptomic signatures of social experience during early development in a highly social cichlid fish

“…During the social experience phase (days 46 and 56), there were no significant transcriptomic differences between the two treatments, which is striking considering the previously described behavioural differences between +F and −F fish observed during the social experience phase (Arnold & Taborsky, ; Fischer et al, ). Moreover, candidate gene studies in rodents showed an effect of maternal separation on gene expression during the phase when early experiences were made.…”

“…Through developmental plasticity, the social environment experienced during the early life of an individual can persistently shape its phenotype (Adkins‐Regan & Krakauer, ; Arnold & Taborsky, ; Feng et al, ; Francis, Diorio, Liu, & Meaney, ; Liu et al, ; Nyman, Fischer, Aubin‐Horth, & Taborsky, ; Taborsky, Arnold, Junker, & Tschopp, ; see review Taborsky, ). For instance, early social experience can influence individual life history decisions (Fischer, Bohn, Oberhummer, Nyman, & Taborsky, ), maternal behaviour (Francis et al, ), learning and memory (Champagne et al, ), mate choice decisions (Adkins‐Regan & Krakauer, ), alcohol abuse (Higley, Hasert, Suomi, & Linnoila, ) and fitness (reviewed in Taborsky, ).…”

“…In vertebrates, the hypothalamus–pituitary–adrenal/interrenal (HPA/HPI) axis has been proposed as a central mechanism responsible for long‐term effects of early social experience (Arnold & Taborsky, ; Banerjee, Arterbery, Fergus, & Adkins‐Regan, ; Fischer et al, ; Francis et al, ; Liu et al, ; Nyman et al, ; Nyman, Fischer, Aubin‐Horth, & Taborsky, ; Taborsky, Tschirren, Meunier, & Aubin‐Horth, ). Hippocampal glucocorticoid receptors (GRs) are implicated in the negative feedback loop controlling glucocorticoid production, which promotes termination of the stress response (de Kloet, ).…”

Heritabilities, social environment effects and genetic correlations of social behaviours in a cooperatively breeding vertebrate

“…However, these behaviours were only loosely correlated on the phenotypic level due to the lack of residual correlations between tests. Previous studies in N. pulcher indicated that helping and submission might represent environment‐induced, plastic alternative social strategies to secure group membership (Bergmüller & Taborsky, ; Fischer et al., ; Kasper, Colombo, Aubin‐Horth, & Taborsky, ). However, in this study not only the genetic, but also the phenotypic correlations between submissive displays and helping were indistinguishable from zero.…”

“…Lack of correlations between behaviours of different tests on the residual level corroborated this supposition. The lack of a phenotypic correlation means that the associations between helping and submissive behaviour are not constrained by regulatory pleiotropy, but individuals can flexibly adjust their levels of helping or submission to the particular environmental requirements (Fischer et al., ; Kasper et al., ). Since there was also no evidence for a shared genetic basis, it is expected that changes in the population mean of helping are unlikely to affect the population mean of submissive behaviour.…”