ABOVE: Genetic material from the Atlantic killifish (Fundulus heteroclitus), shown here, seems to be responsible for helping the Gulf killifish survive in polluted conditions.

ANDREW WHITEHEAD

The population of Gulf killifish in the Houston Ship Channel had been steadily declining for decades, likely a result of the toxins pouring in from industrial activity, when suddenly and mysteriously, in the 1970s, it started trending upwards. The waters hadn’t changed. Over the past six decades, the activity of several refineries and a petrochemical complex has led to large concentrations of halogenated and polycyclic aromatic hydrocarbons (HAHs and PAHs) that are known to disrupt cardiac development—often lethally— in invertebrates.

The quantities found there should be lethal to the killifish, scientists thought, and yet, they’re surviving and even thriving. Fundulus grandis, which only grow to a maximum of seven inches long and are commonly used as baitfish, had somehow adapted and managed to live in the extremely polluted habitat.

Elias Oziolor, a bioinformatics scientist at Pfizer and previously an evolutionary geneticist at the University of California, Davis, wondered how the fish could have evolved so quickly in response to extreme environmental pressures. The answer, he and his colleagues reported in Science on May 3, appears to be genetic mutations brought into the population from an entirely different species of killifish.

Axel Meyer, an evolutionary geneticist at the University of Konstanz who was not involved in the study, says in an email to The Scientist that the suggestion that these fish were able to quickly gain a genetic advantage over pollution thanks to genes from another fish is “thrilling.”

Pollution in the channel radiates outward in a gradient pattern, with dramatically high levels of HAHs and PAHs gradually decreasing on the way to the Gulf of Mexico. When Oziolor decided to investigate how the fish live among these pollutants, the first step his team took was to capture killifish from 12 locations along this gradient. They brought these fish back to a lab at Baylor University in Texas and waited for them to spawn. When they did, the team exposed the embryos to different concentrations of polychlorinated biphenyl 126, an HAH.

The embryos from fish that came from the most polluted areas of the channel avoided cardiac malformations when exposed to concentrations up to a thousand times higher than the fish from areas with less pollution could withstand. When they crossed fish from a polluted area with fish from a less-polluted zone, their offspring had an intermediate level of protection, which the authors say is evidence of a genetic basis for the protection against HAH.

So next they conducted a genetic screen. They found several loci in the genome that seemed to be strongly selected for, meaning they were likely to be helping the killifish survive. These mutations disabled the molecular pathway that normally would lead to cardiac deformities. But “even more surprising,” says Oziolor, was that two of these regions were not coming from genetic variability seen in Gulf killifish. “They were coming from a different species entirely.”

The fish had undergone hybridization—the sharing of genes due to mating between different species. Interspecies mating rarely results in competitive advantages for the offspring, says Oziolor. But in this case, genetic material from the Atlantic killifish (Fundulus heteroclitus) seems to be responsible for helping the Gulf killifish survive in the extreme conditions. The mutations present among Gulf killifish that were protecting against cardiac malformations in the presence of HAH were found among Atlantic killifish, but not among Gulf killifish from less-polluted areas that were still vulnerable to the compound.

Scientists have suspected that mixing genes through hybridization “can benefit populations experiencing rapid environmental change,” Clint Muhlfeld, an aquatic ecologist with the United States Geological Survey (USGS) who was not involved in the study, tells The Scientist in an email. “But to my knowledge this is the first comprehensive study to directly and scientifically support this prediction.”

These five-day-old Gulf killifish embryos were exposed to PCB-126. The one on the right, which comes from a pollution-tolerant population, is developing normally, while the embryo on the left, which comes from a population without as much pollution, has lethal developmental problems. Cole matson/haley davis

How this interspecies mating occurred remains a puzzle. Atlantic killifish are not normally found in the Gulf and are not strong enough to have swum there on their own. Oziolor says he believes their eggs may have been transported by water on fishing boats that traveled from the Atlantic.

Now, he and his team hope to find out just how common it is for these fish to share DNA in other polluted areas of the Gulf. He says the most important takeaway is how important it may be to give species the space to mingle.

“If we fragment habitat,” he says, “it makes it much more difficult for populations to interact with each other and swap genetic material that might prove to be helpful in very dire situations.”

Still, Oziolor emphasizes that humans did not intentionally cause this hybridization, and such mixing could be hazardous. Muhlfeld cautions that “in many cases hybridization driven by human activities, such as translocation of species, tends to occur quickly and reduce fitness, genomic integrity, and ultimately native species diversity.”

E.M. Oziolor et al., “Adaptive introgression enables evolutionary rescue from extreme environmental pollution,” Science, doi:10.1126/science.aav4155, 2019.