Barren environment damages cognitive abilities in fish: Behavioral and transcriptome mechanisms

Abstract

The surrounding environments that animals inhabit shape their behavioral phenotypes, physiological status and molecular processes. As one of the driving forces for the adaptation and evolution of marine animals, environmental complexity has been shown to affect several behavioral characteristics in fish. However, little is known about the effects of environmental complexity on fish spatial cognition and about the relevant regulatory mechanisms. To address this theoretical gap, black rockfish Sebastes schlegelii, which is a typical rock fish species, were exposed to laboratory-based small-scale contrasting environments (i.e., spatially complex environment vs. spatially barren environment) for seven weeks. Subsequently, the spatial cognitive abilities and behavioral performance during captive period were determined, and transcriptome sequencing and analyses for fish telencephalon were conducted. In general, the fish from barren environment had significantly lower spatial learning and memory abilities compared with the fish from complex environment (i.e., the complex fish exited the maze faster). During the whole captive period, the frequency of aggressive behavior among barren fish was significantly higher than complex fish. And meanwhile, the group dispersion index of barren group was also significantly higher than complex group, which indicated that complex fish tended to distribute in a more homogeneous pattern than barren fish. Through transcriptomic analyses, a series of differentially expressed genes and pathways which may underpin the damaged effects of barren environment on fish spatial cognition were identified, and these genes mainly related to stress response, metabolism, organism systems and neural plasticity. However, no significant differences in growth performance, locomotor activity (indicated by swimming behavior and rotatory behavior) between treatments were detected. Based on these results, mechanisms in the levels of behavior and molecule were proposed to explain the environmental effects on fish cognition. This study may provide fundamental information for deeply understanding the environmental effects on marine animals.

Keywords: Environmental complexity; Fish behavior; Learning ability; Sebastes schlegelii; Transcriptomic.