Atlantic tomcods (a type of cod fish) from the Hudson River have some of the highest levels of toxic pollutants like PCBs (polychlorinated biphenyls), PCDDs (polychlorinated dibenzo-p-dioxins), and PCDFs (polychlorinated dibenzo-p-furans) in their livers among the fishes in nature. The Hudson River has several sources of pollution, including accidental sewage discharges and urban runoff. Perhaps more importantly, the General Electric facilities dumped anywhere between 209,000 and 1,300,000 pounds of PCBs into the river from 1947 to 1976.

Outside of having elevated pollutant accumulation in their bodies, Atlantic tomcods from the Hudson River show a 100-fold reduction in sensitivity to pollutants. That is, they produce less detoxification enzyme, P4501A, when they are exposed to PCBs and PCDDs. Their reduced response to pollutants even carries onto their direct offspring. Thus, this trait is possibly heritable, meaning that some sort of evolutionary change could have occurred in the fish population. Isaac Wirgin at the New York University School of Medicine led an investigation into the mechanism behind this adaptation. His findings appear in a recent issue of Science.

When fish are exposed to a PCB, the chemical can bind to a receptor in the cytoplasm called the aryl hydrocarbon receptor (AHR). This AHR-PCB complex then moves into the nucleus of the cell to activate transcription of genes, including that of P4501A, which produces enzymes to metabolize the pollutants. As tomcods from the Hudson River have less activation of P4501A even with high bioaccumulation of pollutants, the researchers reasoned that the AHR is involved. They compared AHR DNA sequences and corresponding protein activities among tomcods from different locales.

While there are two different types of AHRs (simply named AHR1 and AHR2) in fishes, the authors focused on the more functionally active AHR2. When they screened for DNA differences in tomcods from seven Atlantic Coast estuaries, they found the presence of two variant AHR2 alleles (i.e., two alternate forms of the AHR2 gene). Tomcods that are located far from the Hudson River were monomorphic for the AHR2-2 allele; they did not have the AHR2-1 allele at all.

On the other hand, at the Hudson River estuary, the AHR2-1 allele showed up more frequently and was present in both monomorphic and heterozygote tomcods. The AHR2-2 allele had a lower frequency of occurrence, showing up only in heterozygote fish, where the fish possessed one copy of each allele.

There are significant functional differences between the corresponding AHR2-1 and AHR2-2 proteins. AHR2-1 has a 5-fold lower binding affinity to a sample pollutant, TCDD (2,3,7,8-tetrachlorodibenzo-p-dioxin), that the researchers used for binding tests. Such a big difference can explain why tomcods from the Hudson River have less sensitivity to toxicants; their population has a higher frequency of AHR2-1, which expresses the less sensitive protein.

The researchers also found other variations between AHR2 genes of tomcods from the Hudson River and those from other locales. Key differences included a deletion of six DNA bases that causes two amino acids, phenylalanine and leucine, to be deleted in the AHR2 protein in an area that’s 43 amino acids away from the ligand binding domain, where PCBs would bind. The researchers suggest that the two amino acid deletion changes the conformation of the protein, making it less accessible to pollutants.

While the authors have determined that AHR2 genetic variation plays an important role in resistance to high pollutant concentrations, they have not ruled out that other factors contribute to the adaptation, as well.

The genetic variation between tomcods in the Hudson River and fish from other locales indicate that an adaptation has occurred. The high frequency of AHR2-1 allele occurrence could account for why they are resistant to high levels of PCBs and other contaminants. This adaptation happened somewhere between the last 50-100 years, which is a very rapid evolutionary change. The authors cannot obtain a more precise time frame, as archived samples of tomcods were stored in formaldehyde and water, making samples unreliable for detailed DNA analyses. Nevertheless, the researchers’ work indicates that human activities that disrupt natural habitats might lead to rapid evolutionary change in wildlife.

The severely polluted habitat of the Hudson River most likely placed selective pressures on the tomcods, particularly in the embryo stage. Being less sensitive to surrounding pollutants would help embryos and adult fish survive. The researchers propose that there could be accompanying evolutionary costs from this adaptation, such as a heightened sensitivity to other environmental stressors. However, they have yet to find examples of evolutionary costs. Of course, there is the obvious cost to humans, as the bioaccumulation of toxins in these tomcods makes them a bad food source.

Science, 2011. DOI: 10.1126/science.1197296