Density-dependent expression of epitranscriptomic, stress, and appetite regulating genes in Atlantic salmon

Abstract

Intraspecific competition due to e.g., density, has substantial influence on fitness dynamics and life histories, but the underlying physiological mechanisms are often complex, and the molecular basis unclear. Further, designing laboratory experiments to measure physiological responses that reflect natural conditions is challenging. Here, we reared Atlantic salmon juveniles in semi-wild conditions in two naturally occurring densities to investigate the molecular mechanism of density-related changes in the hypothalamus, a key brain region regulating stress and energy homeostasis. We measured density-dependent changes in the expression of 12 genes involved in appetite and stress regulation, and 16 genes involved in post-transcriptional regulation of gene expression via m6A RNA methylation. This gene set includes paralog pairs, to account for potential functional divergence associated with salmonid genome duplication. We also quantified genotype-environment interactions between density and two major life-history loci, vgll3 and six6. We found significant density-related differences in the expression of genes coding for corticotropin-releasing factors, appetite stimulators and inhibitors, and m6A RNA methylation actors. Moreover, a paralogue of an appetite inhibitor showed a density-dependent pattern that was the opposite of what was expected. Six6 locus was also associated with changes in the expression of epitranscriptomic markers, including two writers and one eraser. Our results highlight that individuals response to density in natural conditions is shaped by a complex interplay between stress, appetite and epitranscriptomic pathways in the hypothalamus. In addition, the functional divergence of paralogs indicates a potential role of genome duplication shaping such a response. We emphasize the value of integrating different physiological responses at the molecular level to better understand ecological processes affected by environmental change.