The remarkable adaptability of octopus with new evidence showing they can alter the information copied from their DNA is an example of epigenetics: modification of gene expression by factors “above” the DNA.
But does this undermine Charles Darwin’s theory of evolution by natural selection? As epigenetics becomes a buzzword in discussions of human differences and diseases, this idea has seeped into the popular press and been eagerly adopted by creationists.
Some claim that heritable changes in gene expression that are influenced by environment completely falsify Darwin’s theory, and instead favour Jean-Baptiste Lamarck’s long-discredited idea that advantageous characteristics enhanced by use are passed down to offspring.
But this is a complete misreading, both of what epigenetics is, and of evolutionary theory. It’s a misunderstanding of both Darwin’s and Lamarck’s ideas.
Epigenetics is hardly a new idea, or even a new word.
Conrad Waddington coined the term in 1942, before we knew that DNA was the molecular basis of genes. He proposed that genes are differentially turned on and off by another level of “epigenetic” processes to produce different cells and organs in the developing embryo.
We have many examples of differential gene expression that occur within the lifetime of an animal or plant.
For instance, some human genes are turned on in the brain but turned off in the kidney, others are turned on in the kidney but off in blood.
Some plants can undergo epigenetic changes to make tough leaves when young and then switch to more succulent leaves when older. Long-term shut-down of genes on one X chromosome in female mammals compensates for the presence of only one X in males.
Epigenetics can work at several levels by blocking or enhancing or changing how the DNA is read. This is effected by tacking small molecules onto DNA or its RNA copy. All these processes are controlled by enzymes, themselves products of the DNA.
Some changes in gene action are influenced by the environment. For instance, reptiles such as alligators and some turtles determine sex by egg incubation temperature. This influences the expression of male or female determining genes.
In all these situations, the repressed state of the gene is passed down through cell divisions within a single animal or plant, but is usually reset in eggs or sperm so that it is not transferred between generations.
But we now know of several situations in which an epigenetic state is carried over, at least partially, into the progeny.
For instance, coat colour in mice is partially controlled by small molecules that bind to DNA, and this state is inherited by offspring. In humans, starvation after post World War II seemed to trigger obesity by a mechanism that is inherited in children, and even grandchildren, of malnourished mothers.
Is epigenetic change induced by use or selected?
Lamarck’s views are generally over-simplified but his core idea was that advantageous characteristics are enhanced by use, and that this enhancement can be inherited by offspring.
The classic cited example was a primitive giraffe with short legs and short neck. It had to stretch to reach succulent foliage and developed longer limbs and neck, and this characteristic was passed on to offspring. In this way an organism’s needs would be met in offspring.
A Darwinian view is that proto-giraffes with slightly longer necks and legs ate better, reproduced more successfully and had more baby giraffes who shared their bone-growth genes.
So is epigenetic change induced by use, or selected for? Evidence supports the latter.
Selection may favour enhanced activity of enzymes that add small molecules to DNA and shape their response to environmental cues.
For instance, it is easy to see why a change in gene expression to make tough juvenile leaves that are hard to eat might be an advantage to a vulnerable seedling. Or inactivating a gene on the X chromosome in females might avoid harmful inequality between the sexes.
So the propensity of a gene to be subject to epigenetic modification can be selected, just like any other Darwinian characteristic.
The new evidence on octopus provides a nice example of selection for elevated activity of the editing enzyme, and of “editable” sequences that surrounding edited sites.
These sites are highly conserved between octopus and squid species that show elevated editing, but almost absent in more distant relatives with no editing. They are concentrated in genes involved in the brain and nerve function of octopus, consistent with natural selection for intelligence in these sophisticated creatures.
There is evidence that epigenetic changes are selected in species such as salt marsh plants to produce locally adapted strains that cope with different salinity.
Epigenetic modifications of DNA have also been recorded in locally adapted oak trees. The male-producing temperature in snapping turtle varies to maintain a stable sex ratio across warmer and cooler regions.
There is plenty of evidence that epigenetic modulation in genetic characteristics is selected in animals and plants. These changes exploit existing heritable genetic variation, and are passed on. This allows populations to evolve in response to environmental challenges.
So we can readily incorporate epigenetics as another source of heritable natural variation to explain how populations become different, and ultimately new species arise.
Darwin would have loved it. In fact to cover the possibility that acquired characters might be inherited, he proposed the idea of “Pangenesis” in 1868, whereby tiny parcels (“gemmules”) were passed from somatic to reproductive tissues.
So if it turns out that a flow of information from experience to inheritance provides more variation for natural selection to work on, Darwin was right again.
Jenny Graves a is distinguished professor at La Trobe University, professor emeritus at ANU and thinker-in-residence at the University of Canberra.
Nick Murphy is a molecular ecologist in the department of ecology environment and evolution at La Trobe University.
Neil Murray is an ecological and evolutionary geneticist and an honorary research associate at La Trobe University.