A study published Dec. 9 in the journal Science and funded in part by NIEHS sheds light on genetic variability that may explain the survival of killifish in four polluted environments on the U.S. eastern seaboard. A team led by Andrew Whitehead, Ph.D., an NIEHS grantee at the University of California at Davis (UCD), sequenced the entire genome of nearly 400 killifish from eight sites along the Atlantic coast and reported that changes in genes in the aryl hydrocarbon receptor (AHR) pathway might hold the key to adaptation.
Scientists have been studying geographically distinct populations of Atlantic killifish that survive in polluted waters. Compounds such as polychlorinated biphenyls (PCBs), dioxins, polycyclic aromatic hydrocarbons (PAHs), and heavy metals that contaminate these estuaries are linked with declines in many other aquatic species.
“We’re excited to see these high-impact findings come from the Oceans and Human Health program,” said Tyson, referring to a collaborative program between NIEHS and the National Science Foundation. “This model, developed in a natural setting, provides opportunities for learning more about genes and pathways that can modify sensitivity to common, persistent environmental pollutants.”
Aryl hydrocarbon receptor involved in resistance
Researchers at the Woods Hole Oceanographic Institution (WHOI) collaborated on the new study. With support from the NIEHS-sponsored Boston University Superfund Research Program, WHOI scientists have been working to uncover the genes unique to the PCB-resistant killifish population in New Bedford Harbor, Massachusetts.
Early studies by scientists at WHOI, UCD, and the U.S. Environmental Protection Agency (EPA) made a connection between increased tolerance to PCB exposure and genes in the AHR signaling pathway. AHR-regulated genes in resistant killifish did not respond to PCB exposure. These genes are highly activated by PCB exposure in most fish populations.
WHOI scientists looked more closely at the AHR gene itself and found changes, called single nucleotide polymorphisms, in two of four AHR genes of the New Bedford Harbor killifish population. But the proteins that resulted from these genetic variations showed no apparent differences in responsiveness to PCBs. This finding led the research team to use more powerful genomic approaches to better understand the complex molecular events involved.
In killifish sampled from the four polluted sites, genes encoding AHR and other proteins involved in its signaling pathways showed strong evidence for natural selection. “We have four independent, geographically separated populations of fish, each of which has evolved resistance to industrial chemicals,” said WHOI biologist Mark Hahn, Ph.D., in a WHOI press release. “And in each of these four populations, selection has targeted the same sets of genes from the same molecular pathway, but in slightly different ways.”
The adaptations involved different nucleotide, or sequence, changes, which lead to variations in the activity of the genes. In other words, the researchers found several avenues for evolving resistance to PCB exposure, rather than just one.
Four of the study sites have been contaminated by PCBs, dioxins, or PAHs since the onset of industrial development in the mid-1900s — New Bedford Harbor in Massachusetts, Newark Bay in New Jersey, Elizabeth River in Virginia, and the Bridgeport area of Connecticut. The other four sites are uncontaminated, and scientists sampled fish from those locations to use as controls.
Why not other species
The scientists also asked why this evolutionary advantage has not translated to other species. “Some people will see this as a positive and think, ‘Hey, species can evolve in response to what we’re doing to the environment!’” Whitehead said in a UCD press release. “Unfortunately, most species we care about preserving probably can’t adapt to these rapid changes because they don’t have the high levels of genetic variation that allow them to evolve quickly.”
Although humans have significantly less genetic variation than killifish, this study opens the door to future research on how polymorphisms in such genes may contribute to differences between individuals in sensitivity to chemical exposure.
Citation: Reid, NM, Proestou DA, Clark BW, Warren WC, Colbourne JK, Shaw JR, Karchner SI, Hahn ME, Nacci D, Oleksiak MF, Crawford DL, Whitehead A. 2016. The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish. Science 354(6317):1305–1308.
(David Banks is a postbaccalaureate Intramural Research and Training Award fellow in the NIEHS Receptor Biology Group.)