Unhelpful adaptations can speed up evolution

Guppies moved to predator-free zones show changes in gene activity


GUPPY GAINS Trinidadian guppies from the Guanapo River basin (shown) make unhelpful changes in gene activity when they first enter a new environment. Those missteps speed up evolution, a new study suggests.

Pierson Hill

When organisms enter a new environment, they’re bound to make some missteps. A new study suggests those initial flubs may speed up evolution.

Trinidadian guppies transplanted from predator-infested waters to streams devoid of predators responded by changing activity of some genes in the brain. Although some changes were helpful, most were disadvantageous. But genes that got off on the wrong foot by changing activity in unhelpful ways evolved the fastest, researchers report September 2 in Nature.

“When the environment has a nurturing effect that’s helpful to you, you don’t have to evolve,” explains lead author Cameron Ghalambor, an evolutionary ecologist at Colorado State University in Fort Collins. But when the environment prompts unhelpful gene activity responses, organisms are forced to change their DNA to compensate, he says.

Scientists have debated how important plasticity — the ability to change traits in response to environmental influences — is for driving evolution, says evolutionary biologist Carl Schlichting of the University of Connecticut in Storrs. Researchers have previously found that helpful, or adaptive, trait changes can be made permanent with DNA mutations. But the new study demonstrates that nonadaptive alterations are the ones that really drive evolution, at least when organisms first move into a new environment, says Schlichting, who was not involved in the study.

Ghalambor and colleagues took guppies (Poecilia reticulata) from a part of the Guanapo River in Trinidad where the little fish are regularly eaten by pike cichlids. The researchers moved the guppies to two streams without cichlids.

After a year, the guppies had produced three or four generations. The researchers then captured some of the fish from both safe streams as well as guppies from the original location rife with predators, plus guppies that lived in a stream historically free of predators. In the lab, researchers bred each guppy group for two more generations. Second-generation fish from each location were split into two groups of siblings. One sibling group’s water supply first passed through a tank containing cichlids that were fed two nonexperimental guppies a day. That water contained chemical signatures of the cichlid predators and distress pheromones from the dinner guppies.

PATTERNS OF CHANGE Guppies transplanted from a part of the Guanapo River where cichlids prey on the small fish to streams free of predators evolved different gene activity patterns (blue). Those patterns are more similar to guppies from a low-predator stream (green) than to fish that stayed in the high-predator region (red). Dots connected by solid lines indicate individual families from each population. C.K. Ghalambor et al/Nature 2015

Researchers then analyzed the activity of more than 37,000 genes in the guppies’ brains. Gene activity patterns distinguished fish from the high-predator river from those that came from low-predator streams. Guppies transplanted to the two predator-free streams had similar gene activity patterns. But those patterns differed from those in fish from the high-predator and low-predator streams.

The researchers found 135 genes that changed activity in the same way in both groups of transplanted guppies. Those changes made the transplanted fish more similar to low-predator than high-predator guppies, indicating that those genes were influenced by natural selection. If random chance rather than natural selection was at work, the genes’ activity changes would not have matched up so neatly, says Schlichting. And if the fish hadn’t evolved, their gene activity patterns would still resemble those of the high-predator guppies.

To determine if the gene activity changes were adaptive, researchers compared siblings raised in tanks that got the cichlid-tainted water to guppies that didn’t get the predator cues.

Of the 135 evolved genes, 120 (89 percent) changed gene activity in response to predator cues in unhelpful ways, the study found. Only 15 genes altered their activity in helpful ways, and those changes were usually small. The results indicate that plasticity can be important for evolution, but not because it helps organisms adjust to the environment right away. Instead, nonadaptive plasticity may force natural selection to work harder on misbehaving genes and to select DNA mutations that help organisms survive. Those DNA changes should increase fitness over the long haul, the researchers theorize.

The study’s strength stems from the large number of genes the researchers analyzed, says Gregory Grether, an evolutionary ecologist at UCLA. Many studies focus on one particular trait, but analyzing many genes allows the researchers to pick out global patterns of evolution, he says. It’s clear that nonadaptive changes fueling natural selection isn’t a fluke, Grether says. “This is the predominant pattern.”

PREDATOR PERIL Cichlids (one shown) prey on guppies. Guppies transplanted to streams free of these predators evolve different gene activity patterns than do fish constantly in danger of being eaten. Paul Bentzen

How the gene activity changes influence behavior isn’t known, and the researchers haven’t tracked down the DNA changes that natural selection presumably favors in the guppies, Ghalambor says.

It will be important to understand how the environment causes these changes in gene activity, and which physiological systems are affected, says geneticist Gene Robinson of the University of Illinois Urbana-Champaign.

Nonadaptive plasticity may spur evolution in the short term, but may not be a driving force in later generations, Ghalambor says. The pattern may also hold only for organisms entering a more benign environment. When the researchers tried the opposite experiment, transplanting fish from low-predator streams to high-predator locations, the transplanted guppies were quickly wiped out. Says Ghalambor: “Extinction is an option.”

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