Transcriptomic and Methylomic Analyses Show Significant Shifts in Biosynthetic Processes and Reduced Intrapopulation Gene Expression Variance in PAH-Adapted Atlantic Killifish

Environmental
contaminants pose a significant selection
pressure
across taxa, potentiating evolved resistance to chemicals. However,
rapid evolution may alter molecular and physiological homeostasis
leading to trade-offs. To elucidate molecular underpinnings of evolved
chemical resistance, we compared liver gene expression and methylation
profiles in polycyclic aromatic hydrocarbon (PAH)-adapted Atlantic
killifish (Fundulus heteroclitus) in
the Republic site (RP), Elizabeth River, Virginia with PAH-sensitive
Kings Creek (KC) fish. We found 1607 differentially expressed and
2252 alternatively spliced genes between RP and KC, with highly enriched
genes involving lipid and amino acid metabolism, respectively. While
308 genes had differentially methylated regions, only 13 of these
genes were differentially expressed. The aryl hydrocarbon receptor
2b gene (ahr2b) was differentially methylated and
expressed, as well as alternatively spliced signifying its critical
role in mediating PAH tolerance. Notably, the intrapopulation coefficient
of variation (CoV) was lower in 82% of 17,566 expressed genes in RP
fish compared to KC fish. Among other pathways, these genes with low
CoV were highly enriched in bioenergetic processes inferring reduced
metabolic physiological variation as a population in RP fish. Altered
metabolic gene expression and overall reduced gene expression variance
in RP fish warrant further studies on fitness trade-offs including
altered susceptibility to other stressors associated with rapid adaptation
to anthropogenic pressures.