Ghost of Lamarck: Working Epigenetics into Evolutionary Theory - Evolution News & Views

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Ghost of Lamarck: Working Epigenetics into Evolutionary Theory

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Epigenetics is a reality that can no longer be ignored. Too many studies have shown that factors above the DNA code are not only influential in trait formation, but can be passed on to offspring. Is this a bridge too far for Darwinian evolution, or can they just extend their theory to encompass "epimutations" to the epigenetic codes?

In January, Science Magazine called Michael Skinner "the epigenetics heretic" for maintaining that chemicals can cause changes in gene expression in mice that persist across generations. Notice who Jocelyn Kaiser says had the biggest knee-jerk reaction of all:

Michael Skinner is gleefully listing the disciplines that he's ruffled with his contention that, without altering the sequence of DNA, certain chemicals can cause harmful health effects that pass down generations. Toxicologists are so outraged that they have tried to block his funding, he says. Geneticists resist having their decades-old understanding of inheritance overturned. Then there are the evolutionary biologists, who have "the biggest knee-jerk reaction of all."

Skepticism is to be expected, Skinner acknowledges: "This is probably going to be the biggest paradigm shift in science in recent history," he declares. (Emphasis added.)

Opinions differ about whether Skinner is a "pioneer who has uncovered a new and exciting potential driver of evolution," or a troublemaker with an "uncompromising personality" some find "cavalier." He seems to enjoy his reputation as a maverick, but is no lightweight; the Smithsonian honored him with an "American ingenuity" award, awarded to ten people who "are having a revolutionary effect" on their fields.

One of those effects is shaking up evolutionary biology. In his original study, his team's paper said, "The ability of an environmental factor (for example, endocrine disruptor) to reprogram the germ line and to promote a transgenerational disease state has significant implications for evolutionary biology and disease etiology."

At the time, skeptics were unconvinced; others were unable to replicate his experiments (but Skinner claims they didn't follow his protocol). More teams are still trying to resolve lingering doubts, but few are considering it a "goofball" idea.

Nature mentioned the Skinner controversy, adding stories from other researchers finding "trans-generational epigenetic inheritance" in mice and plants. "The roots of inheritance may extend beyond the genome, but the mechanisms remain a puzzle," Virginia Hughes says. The mysteriousness of it all is the only token she offered to bust the ghost of Lamarck:

The subject remains controversial, in part because it harks back to the discredited theories of Jean-Baptiste Lamarck, a nineteenth-century French biologist who proposed that organisms pass down acquired traits to future generations. To many modern biologists, that's "scary-sounding", says Oliver Rando, a molecular biologist at the University of Massachusetts Medical School in Worcester, whose work suggests that such inheritance does indeed happen in animals. If it is true, he says, "Why hasn't this been obvious to all the brilliant researchers in the past hundred years of genetics?".

Maybe it has been obvious. Hughes mentions Linnaeus as an early eyewitness.

In the 1740s, he received a plant specimen that looked very similar to common toadflax (Linaria vulgaris), but with very different flowers. Linnaeus was shocked because this challenged his theory that plant species could be categorized by the structure of their flowers. "This is certainly no less remarkable," he wrote, "than if a cow were to give birth to a calf with a wolf's head." He named the plant Peloria, after the Greek word for 'monster'.

It wasn't until the 1990s that methyl groups on a gene implicated with the "monster" flowers were shown to completely shut the gene down. Epigenetics started coming into prominence in the early 2000s. Today, it remains "a huge black box" for biologists. "This idea of an environmentally responsive genome still stirs debate," Hughes writes. "But the notion that epigenetic marks are transmitted across generations is even more provocative." For instance, Nature describes third-generation mice that inherited a fear of acetophenone their great-grandfathers had been trained to fear, even when the young mice had never been exposed to it.

Scientists are exploring hypotheses involving methylation, histone tags, RNAs and even prions to try to understand what's going on. In Science Magazine, researchers in France and the Netherlands published new work into "Mapping the Epigenetic Basis of Complex Traits." Their approach tries to extend neo-Darwinism into variations in "differentially methylated regions" (DMRs), that they say "act as bona fide epigenetic quantitative trait loci (QTLepi)" -- markers that could be acted on by artificial or natural selection. These "epimutations" might account for "missing heritability" and "may thus provide an epigenetic basis for Darwinian evolution independently of DNA sequence changes."

In a Perspective piece about this paper in Science, Robert J. Schmitz is hopeful: "These results provide strong evidence that epialleles contribute to the heritability of complex traits and therefore provide a substrate on which Darwinian evolution may act."

But can neo-Darwinism survive by simply adding "epi-..." to every concept in the theory? "This possibility may have deep implications on how we delineate and interpret the heritable basis of complex traits," they state in conclusion. So far, though, they have only experimented with artificial selection -- a form of intelligent design -- and only on two traits in the lab plant Arabidopsis. They could not demonstrate whether "epimutations" are randomly produced in the wild or are subject to natural selection. Some of the DMRs they produced overlap with wild type, but they could be missing something: "Therefore, these epiRIL DMRs may have been historical targets of epimutations in the wild, either through trans-induced ddm1-like mutation events or else through still unknown mechanisms."

Schmitz admitted that "The detected epialleles from all of these populations, whether experimental or natural, arose in the absence of experimental environmental perturbation." It was a contrived scenario, therefore, with only a suggestion of possible relevance to Darwinian evolution. He continues:

The possibility of environmentally induced epiallele formation and its role in local adaptation to changing environments has generated considerable interest, but there is currently limited evidence to support the existence of these environmentally induced transgenerationally stable epialleles. An important next step will be to determine if the environment can affect the rate at which these spontaneous epialleles appear.

An alternative possibility, though, is that genomes harbor pre-coded responses to environmental change. "Cortijo et al. also uncovered a sizable number of allelic variants in natural populations that are silenced by DNA methylation," Schmidt notes. "The method used to create the epiRIL population led to the reactivation of some of these alleles, which resulted in heritable phenotypic variation." That's stunning; it's as if the variants were waiting in the wings, ready to fly into action. Where did the variants come from? Why were they silenced? Wouldn't natural selection get rid of them, if they were useless? A scientist attuned to design might think like a programmer: these could be variations in code that can be switched on when needed.

In the face of the epigenetics revolution, Darwinian evolutionists are not throwing in the towel. In January, Sujata Gupta suggested in Nature News that epigenetics is "important for evolutionary success." She writes, "Although biomedical researchers have been investigating the links between epigenetics and human health for some time, evolutionary biologists are just beginning to take up the subject." Epigenetics might be a method for invasive species to thrive, for instance. Our friend Jerry Coyne is repulsed by the suggestion:

Some critics aren't ready to accept the links between epigenetics and invasive species. Jerry Coyne, an evolutionary geneticist at the University of Chicago in Illinois, says their success can be explained by well-established evolutionary theories. Sometimes a species moves into an unoccupied niche, and sometimes a small amount of genetic diversity goes a long way. "It doesn't have to have a lot of variation to evolve," he says. "We have perfectly good other reasons, which are based on more solid premises, on why invasive species succeed."

Sounds like classic Coyne: nothing to see here; evolutionary theory is still standing strong. Gupta, however, predicts that "research into ecological epigenetics is poised to take off." She provides no potential reconciliation with neo-Darwinism.

In the middle of a scientific revolution, you can't predict how things will eventually shake out. As work continues into this unexpected turn in genetics, we can only speculate about the impact on evolutionary theory.

If the genome consists of multiple levels of coding, if code can be silenced and reactivated, and if the genome can reprogram itself by cues from the environment, then Darwin's 1859 hypothesis, even after its 1930s update, "neo-Darwinism," looks simplistic and antiquated. Clearly, the environment has no ability to cause adaptive effects, let along program or reprogram anything. Instead, the adaptability of the genome appears more like a design feature: a mechanism for the genome to remain robust through environmental perturbations.

Design thinking has taken the lead in the epigenetics age. We expect it to continue to do so.

Image source: THEfunkyman/Flickr.


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