Neuromolecular signatures of fish social interactions under normal and climate change conditions

Abstract

Coral reef fish exhibit a large variety of behaviours crucial for fitness and survival. The cleaner wrasse Labroides dimidiatus displays cognitive abilities in its interaction with other species by providing services of ectoparasite cleaning. These features serve as a good model to understand the complex processes of social behaviour and how these interactions might be altered by changes in the marine environment due to ocean acidification (caused by elevated CO2) and warming (elevated temperature). In general, little is known about the functional molecular basis of cooperative behaviour between L. dimidiatus and its potential client fishes and how rapid environmental changes might affect it. Thus, here we investigate the molecular mechanisms responsible for the interaction behaviour using Acanthurus leucosternon as client. In addition, we exposed interacting fish species to three conditions representing predicted future climate change conditions (according to RCP8.0 2100) and compare with a control of present-day levels of temperature and CO2 :1) elevated levels of pCO2 (1000 μatm), 2) elevated temperature (32oC), and 3) a combined condition of elevated levels of CO2 and temperature. We dissected the fore-, mid-, and hindbrain regions of each fish to analyse specific differential gene expression, using transcriptomics, and we found that most of the variation and transcriptional response in both species was regulated in the hindbrain and forebrain regions. The interaction behaviour responses of L. dimidiatus during ambient environmental conditions involved immediate early gene alteration, dopaminergic and glutamatergic pathways, the expression of neurohormones (such as isotocin) and steroids (e.g. progesterone and estrogen), as well as social decision-making genes. In contrast, for the client, fewer molecular alterations were found, mostly involving pituitary hormone responses. However, the molecular signatures of L. dimidiatus were affected in all future climate change conditions with transcriptional changes observed in functions such as stress response (i.e. hypoxia, apoptosis, heat shock proteins), histone regulation, metabolism and the synapse. Key molecular processes, such as learning and memory activation in the cleaner wrasse and stress relief and reduced aggression in the client, were affected by the future climate change conditions. Genes involved in behaviour and memory were altered in expression under the elevated CO2 and temperature conditions, whereas the combined condition showed no expression changes related to behaviour, suggesting no additive effect on the cognitive abilities of L. dimidiatus with two simultaneous conditions. Hence, future environmental conditions influence the molecular programming involved in the mutualism maintenance for L. dimidiatus and its potential clients with possible large-scale effects on the coral reef ecosystems.