Benchmarks: February 12, 1809: Charles Robert Darwin is born - and so began modern biology

by Nicole Branan
Thursday, January 5, 2012

During his five weeks in the Galapagos Islands, Darwin collected many samples, some of which are shown in the traveling Darwin exhibit. Denis Finnin, American Museum of Natural History

As celebrations in honor of Charles Darwin’s 200th birthday are in full swing this month, a revolution is rumbling through evolutionary biology. In the 150 years since Darwin published his landmark book “On the Origin of Species,” scientists have elucidated much of the molecular underpinnings of how evolution — natural selection, punctuated equilibrium and the like — works. One of the pillars of evolutionary theory has long been the notion that the DNA sequence is the only molecular information that is passed on from one generation to the next. But over the last decade or so, an avalanche of studies has shown that epigenetic settings — specific markings on the genome that can turn a gene on or off — can be heritable as well. Moreover, some of these epigenetic changes are triggered by environmental influences, such as stress or diet, suggesting that there is much more to evolution than just random variation followed by selection of the fittest.

Darwin knew that organisms pass certain traits on to their offspring, but he didn’t know how. Several decades later, genetics clarified the process: Random mutations and genetic shuffling during reproduction can change traits and then over time, those traits that make an individual more competitive become more common in future generations — or so scientists thought.

The first inkling that this model was only part of the story came in the 1990s when scientists looked at a batch of young water fleas that grew larger heads to avoid being eaten when they sensed that a predator was around. Such an early developmental change in response to environmental conditions was not unusual, but it turned out that subsequent generations had large heads as well, even when no predator was there. “That was one of the key things that alerted us that here is an effect that is caused by the environment, which is then inherited for a few generations,” says Scott Gilbert, a biologist at Swarthmore College in Pennsylvania. It turned out that other studies throughout the 20th century showed such epigenetic inheritance as well. And in 1995, Eva Jablonka, an evolutionary biologist at Tel Aviv University in Israel, and Marion Lamb, a geneticist at the University of London in the United Kingdom, documented about 40 cases.

The fact that organisms develop differently according to environmental cues and that epigenetic changes are responsible is neither new nor surprising. Changes in epigenetic settings modify genes: For example, certain environmental cues sometimes trigger the tagging of DNA with methyl groups, tiny chemical attachments that can silence a gene. “If you have a tree that is growing on a hilltop where there is a lot of wind, it’s going to be stunted and a little bit thicker than the genetically identical tree that is living in a valley and doesn’t get a lot of wind,” says Eric Richards, a biologist at the Boyce Thompson Institute for Plant Research at Cornell University in Ithaca, N.Y.

But unlike a genetic mutation, the changes in epigenetic settings do not alter the actual DNA sequence. Therefore, scientists assumed epigenetic changes weren’t passed down from generation to generation. So, the offspring of the stunted tree would grow to a normal size if it grew in an area with little wind. “Everything is reset,” Richards says, “and the next generation does it all again depending on the environment it lives in.”

The realization that offspring inherit at least some epigenetic changes turns this idea on its head because now, with an epigenetic change, you can genetically inform your kids about the environment you were in, says Oliver Rando, a biochemist at the University of Massachusetts in Worcester.

That has important implications for how scientists think about evolution because it opens up a potential new avenue for adaptation, Jablonka says. It allows organisms to adapt to rapidly changing environments — an environment that may change in as few as two generations, Jablonka says. The idea that the environment makes an adaptive, and therefore beneficial, change that can be inherited is “a rather large departure from the traditional idea of how evolution works,” Richards notes.

Traditional evolution is supposed to happen based on random, non-directed genetic changes and then selection does the rest of the work. So, does the discovery that individuals can inherit more than just their parents' DNA sequence mean that it is time to rewrite the textbooks? Not so fast, Richards says. Right now, he says, it’s not clear whether the epigenetic phenomenon actually matters, because it isn’t clear whether epigenetic changes push an organism down a specific path or whether those changes are just random, just as DNA mutations are random. “Some evolutionary biologists say, ‘If it’s random then it doesn’t change [our understanding of how evolution works] … because selection still has to act on it,'” he says. “So, saying epigenetic variation may be important and, worse yet, saying it’s not random, and, worse yet, saying that it’s not only directed by the environment but that it actually could be adaptive — that’s where it gets controversial.”

However, even random epigenetic changes could still affect the evolutionary process because they can change mutation rates, Jablonka says. Certain epigenetic settings can, for example, undermine repair mechanisms that normally would police genes and fix mutations. Take the case of male mice treated with a fungicide called vinclozolin. These mice produce offspring with reduced fertility because of an epigenetic change associated with the fungicide that scientists have shown is heritable. However, this change is unlikely to be adaptive, Rando says. “Why it would make sense in the wild for an animal that [is affected by] this molecule to have kids who have fewer children isn’t really clear.”

Another question is how long epigenetic changes last. When trying to figure out how common epigenetic inheritance is, Jablonka found 101 cases in which epigenetic changes survived for two or more generations. But in the real world, “you are looking at very long time frames when you are talking about evolutionary change, and if you do genetics in the lab, you are looking at five, six, maybe 10 generations, and that is sort of a flash in the pan,” Richards says. But at least one epigenetic variant — the symmetric form of the toadflax plant — has been around since 1742, Gilbert points out, so at least it’s possible for epigenetic changes to last for dozens of generations. Nonetheless, like other questions in evolution, it’s difficult to follow epigenetic changes in long-lived organisms over long periods in the lab because such experiments would take decades, if not centuries.

The question is, “if epigenetic changes only last a couple of generations, does that matter?” Richards says. Jablonka says it does, partly because environmentally induced epigenetic changes can speed up the evolutionary process by targeting a lot of individuals at once. “It’s not just one individual with a random mutation; instead it’s almost the entire population that is able to respond epigenetically.”

Thus environmental changes, such as those that may come as the global climate changes, could lead to epigenetic changes in large populations. “I think that what is happening now to the theory of hereditary evolution is to some extent similar to what happened to it when Mendel’s laws were rediscovered,” Jablonka says. “It changed evolutionary biology and I think that we are at a similar point now.”

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