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.