Do Organisms Become More Evolvable in Times of Stress?

Regis Duvignau / Reuters

Updated on November 18, 2015

Imagine that you wake up in a pit, surrounded by people who are all wounded and bleeding. Something had clearly gone horribly wrong. Maybe you panic. Maybe you tend to the wounded. Maybe you team up to plan an escape. But if you’re a red flour beetle, you do none of those things. Instead, you quietly become more evolvable.

When Joachim Kurtz from the University of Münster placed healthy beetles among wounded peers, he found that they can unveil mutations that are present in their genomes but whose effects are usually masked. By exposing these hidden mutations, the beetles don’t gain any benefits themselves, but they increase the odds that the next generation will be better adapted to the challenges are at hand.

Here’s how it works. Genes contain instructions for making proteins—molecules that fold into complex three-dimensional shapes. Mutations in the genes can change the shape of the resulting proteins, which affects how well they work. But even if a mutation can change the shape of a protein, that doesn’t mean it will.

Whether it will depends upon HSP90, a protein that helps other proteins to fold.  Think of HSP90 as the head of an origami school: It’s stuffy and old-fashioned, strictly enforcing a traditional style upon its students. They might be tempted to try something new, but HSP90 won’t let them. So, despite their individual proclivities, their works all look the same. Now, if you fire HSP90, the students get to exercise their full creative streak, carrying out new innovative folds and producing a diverse range of protein creations.

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This is, in fact, exactly what happens to animals under stressful conditions. In the 1950s, a scientist named Conrad Waddington exposed the pupae of fruit flies to heat or chemicals, and found that the insects emerged with weird features like extra body segments or misshapen wings. These results went unexplained until 1998 when Susan Lindquist at the Massachusetts Institute of Technology depleted HSP90 in flies, and found that they grew up with the same kind of deformities. Their genes hadn’t changed; Lindquist (and Waddington before her) had simply unmasked genetic variation that was already there, allowing it to physically manifest.

Lindquist's team has since found that HSP90 stores genetic variation in bacteria, plants, yeast, and animals. Recently, they showed that it probably drove the evolution of blind cavefish, helping to shrink their eyes in dark caves when sight is no longer valuable.

These studies suggest that HSP90 is a major driving force in evolution, a way of tuning an organism’s evolvability. By allowing mutations to build up behind the scenes and releasing them all in one burst, it produces a sudden bonanza of new traits that natural selection can act upon. The poorer ones get weeded out, and the better ones to flourish.

Waddington and Lindquist showed that this process can be triggered by stressful situations like heat. But Kurtz showed that social information about stressful situations can do the same. When he housed red flour beetles in jars with others that were leaking fluids from needle wounds, the uninjured insects weren’t themselves stressed. They didn’t switch on any stress-related genes. But they reacted to the signs of danger around them by switch on immune-system genes and by turning down the production of HSP90. “We were very skeptical that this would happen,” says Kurtz.

“This is the first demonstration that the level of HSP90 can be regulated by environmental context,” says Clifford Tabin, who co-led the cavefish experiments.

“The data are really startling!” says Daniel Jarosz from Stanford University, who has also worked extensively on HSP90. “They suggest that Hsp90 activity is tuned to a far broader array of environmental stimuli than could previously have been imagined.” Still, he notes that Kurtz’s team haven’t drawn any explicit links to evolvability. They don’t know if the changes in HSP90 translate to “real-world evolutionary change.”

That’s what Kurtz now wants to understand. When the beetles share space with injured comrades, what are they responding to? Something visual? Chemical? Physical interactions? How exactly do those potential sources of information affect the levels of HSP90? Do other animals react in the same way? And perhaps most importantly, do the beetles produce more varied or better-adapted offspring as a result?

These are tough questions to answer. “You need to check a lot of animals for subtle physiological or behavioral changes that are difficult to find,” says Kurtz. In other words, he has to play the part of natural selection itself. And that’s a tough role to understudy.

Meanwhile, the study has come under criticism from other evolutionary biologists. Graham Coop from the University of California, Davis, summed up some of the common criticisms on Twitter, noting that in studies about hidden mutations, “the evolution side of the story is often weak.” For example, in both the beetle and cavefish studies, “would populations really evolve that much slower without this extra variation?” Artificial selection experiments, in which people have deliberately bred animals with specific traits, have shown that populations can evolve very rapidly through “bog-standard heritable variation”. “Why then do we need to evoke elaborate mechanisms to supply that variation, and why would such mechanisms evolve?” he asked.