Charles Darwin was a firm believer in the inheritance of acquired characteristics. In his book The Variation of Animals and Plants Under Domestication, Darwin gave many examples of the hereditary transmission of adaptations. He also published an account in Nature about dogs with an inborn fear of butchers. Their father had a violent antipathy to butchers, probably as a result of being mistreated by one, and this fear was transmitted not only to his children but also to his grandchildren.

Darwin knew nothing of genes or random mutations, which only became part of biology in the twentieth century. He put forward his own theory of heredity in the The Variation of Animals and Plants Under Domestication, entitled ‘The Provisional Hypothesis of Pangenesis.’ In order to understand, for example, how a dog could inherit something a parent had learned, or how a plant’s descendants could inherit its adaptations to a new environment, Darwin proposed that cells all over the body threw off microscopic ‘gemmules’ which somehow entered the egg and sperm or pollen cells, transforming them to make these characteristics hereditary.

The great French naturalist Jean-Baptiste Larmarck proposed decades before Darwin that habits could be inherited, and in this sense Darwin was a Lamarckian. Darwin’s theory of pangenesis was largely ignored, and was airbrushed out of twentieth-century hagiographies of Darwin. In twentieth-century biology, Lamarckian inheritance was treated as a grave heresy in the West, where Neo-Darwinism predominated. In the Soviet Union, by contrast, the inheritance of acquired characteristics was orthodox, which only intensified the prejudice against it in the capitalist world. Neo-Darwinism differs from Darwinism in attributing heredity to chemical genes, which can only change by random, purposeless mutations, and in denying the inheritance of acquired characteristics. Many neo-Darwinians are unaware that Darwin himself had very different views. Darwin was not a neo-Darwinian.

The selfish gene theory, advocated most strikingly by Richard Dawkins, took the neo-Darwinian world-view to an extreme. The genes were personified: Dawkins argued that they were selfish, and as ruthless as Chicago gangsters. They had the power to ‘mould matter’ and ‘create form.’ The genetic material, DNA, was no longer a mere molecule: it was animated and purposive. Ironically, Dawkins persuaded many of his readers that life was purposeless and mechanistic by using vitalist rhetoric, attributing minds and purposes to DNA molecules. But behind the haze of misleading metaphors about selfish molecules, he was popularizing the standard neo-Darwinian theory that evolutionary creativity occurred only by random mutations, with no purpose or direction. Evolutionary change was driven by the changes in gene frequencies in the population as a result of natural selection. Acquired characteristics could not be inherited.

Unfortunately for Neo-Darwinism, the facts do not fit the theory. The taboo on the inheritance of acquired characteristics was lifted at the beginning of the twenty-first century, with the recognition of epigenetic inheritance, meaning inheritance over and above the genes. Some kinds of epigenetic inheritance depend on small RNA molecules (sRNA), others on the methylation of DNA, others on modifications to the proteins that bind to DNA. The genes are not changed through mutation, but are switched on or off through the way they are packaged. The discovery that some of these changes are inherited through eggs, sperm and pollen marks a revolutionary change in modern biology.

Some remarkable recent studies have shown that mice can inherit their fathers’ fears, reminding us of Darwin’s report of dogs with an inherited fear of butchers. In these experiments, carried out by Brian Dias and Kerry Ressler, males were exposed to the smell of a chemical called acetophenone that they would never normally encounter in nature. They were given mild electric shocks when smelling this chemical, and soon became frightened when they smelled it again. This was a classical Pavlovian conditioned reflex. However, their children and grandchildren were also terrified of the smell of acetophenone. They were affected even when the fearful fathers’ sperm was transmitted by artificial insemination, preventing any form of cultural contact.

How could fearful responses to a smell be transmitted from noses and brains to sperm cells? Dias and Ressler suggest that molecular influences travelled through the blood stream. This sounds very like a modern version of Darwin’s gemmule hypothesis. In plants, too, there is now good evidence that sRNA molecules can move from various organs of the plant through the sap to the eggs and pollen, bringing about heritable changes that continue over generations.

To what extent can the fears of human fathers be transmitted to their offspring, even in the absence of any contact between the fathers and their children? No one knows.

Much remains to be discovered about epigenetic inheritance. But it is already clear that evolutionary theory needs to be extended or revised. The dogmas of Neo-Darwinism have been superseded. Not surprisingly, this is the subject of a lively debate within contemporary biology.

As evolutionary theory moves beyond the narrow confines of Neo-Darwinism, the question of evolutionary creativity is once again thrown open. The inheritance of learning and adaptations does not depend on random genetic mutations, but on direct transmissions from parents to offspring. Hence the creative responses of organisms to challenges are a major source of evolutionary creativity, just as Darwin thought, and as Lamarck thought before him. Darwin attributed these adaptive abilities to the ‘co-ordinating power’ inherent in living organisms. But he did not explain how this power worked, and we still do not know. But we do know that organisms themselves can be creative, and that some of their learning and adaptation can be passed on to their descendants. Evolution can happen faster and more purposefully than twentieth-century biologists allowed them to think.