Some fish evolve to survive the most poisoned places in America

Virginia's Elizabeth River is a toxic cocktail of industrial pollutants: PCBs, which cause skin ailments and birth defect; PAHs, which have been linked to cancer; dangerous heavy metals like arsenic and lead; smoky-smelling creosote. Formerly the site of a wood treatment facility and a Navy sludge dump, the river is now on the EPA's Superfund list, identified as one of the most hazardous waste spots in America.

Few creatures would want to live in those waters. But that's exactly what thousands of Atlantic killifish do.

In a study published Thursday in the journal Science, researchers report that four distinct populations of killifish, living in four Superfund sites on the East Coast, have separately and rapidly evolved a genetic adaptation that allows them to survive in severely contaminated waters. They likely were able to do so because they were already so abundant, which made it easier for them to evolve.

[For a few Alaska fish, 1964 earthquake spurred rapid evolution]

Their success illustrates a sad fact about evolution and environmental change, said co-author Andrew Whitehead, a biologist at the University of California at Davis: The least vulnerable species are best positioned to survive.

"Who are going to be the winners and the losers in rapidly changing environments?" he asked. "The winners are the species with more good cards to play."

Short, squat and tiny killifish, also known as mummichogs or mud minnows, are masters of marshes and coastal estuaries. Killifish swim together in massive shoals – their Narragansett name literally means "going in crowds" – and are some of the most abundant fish in North America. They've also evolved to be extremely resilient, capable of withstanding the dramatic shifts in temperature, salinity and dissolved oxygen that occur in their habitats as tides go in and out.

But under ordinary circumstances, they struggle to cope with environmental pollutants: If you dropped an average killifish into toxic waters, it wouldn't last very long.

That's why ecologists have puzzled over the populations that persist in the Elizabeth River, as well as in New Bedford harbor in Massachusetts, the waters around Bridgeport, Conn., and New Jersey's Newark Bay – all former industrial sites now on the Superfund list. The fish there are able to withstand levels of pollution 8,000 times higher than the normal lethal limit. Clearly, they've had some adaptation that the rest of their species lacked. What was it?

To find out, Whitehead and his colleagues sequenced the genomes of nearly 400 killifish from those four spots and four non-polluted areas nearby. The fish from the Superfund sites shared a set of mutations on a part of the genome related to a signaling pathway called aryl hydrocarbon receptor (AHR). The pathway regulates the immune system and release of the hormone estrogen, and, most importantly, it mediates toxicity. It's what makes killifish sensitive to pollutants. But without AHR, they can swim in toxic waters without getting hurt.

It's unusual for animals like killifish – which have life spans of years, not months – to evolve so rapidly, especially in four separate spots. To Whitehead, that suggests the mutation for the AHR deletion already existed in the larger killifish population, lying dormant like a superpower the animals didn't know they had. Once the changing environmental circumstances made the mutation useful for fish in polluted spots, it rapidly spread to the rest of the community. In real time, the animals evolved to adapt to their poisoned habitat.

But this is not a happy story. For one thing, scientists don't yet know whether there's a cost to the AHR mutation in killifish.

"If you disable this pathway, how does that effect estrogen and immune signaling?" Whitehead wondered. "That's the million-dollar question … and the answer isn't clear yet."

More significantly, though, most creatures won't be as lucky as the killifish.

Humans are changing ecosystems in matters of years, while most vertebrate evolution happens over the course of millennia, if not longer. When environmental shifts happen fast, animals can't wait around for the right, helpful mutation to occur, especially if they're animals with long life spans that don't reproduce very rapidly. They have to hope that this mutation already exists in the population, waiting to become useful.

The latter scenario is more likely to happen when the population in question is larger and thus contains a larger degree of genetic diversity. The killifish population is one of the biggest.

"Killifish top the charts in terms of vertebrates," Whitehead said. "That's probably what stacked the deck in their favor."

The situation holds a certain "tragic irony," he said. Species that harbor large numbers of organisms and huge amounts of genetic diversity – think bugs and bacteria – are most able to adapt to new and deadly poisons. Unfortunately, those are usually the species that we're trying to tamp down. Meanwhile, populations humans hope to save, because they've been decimated by hunting or habitat loss, are least equipped to evolve.

"There's a critical level of genetic diversity that's necessary for the adaptive potential of species," he continued. Most endangered species, by virtue of being endangered, don't have it.