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Gentry had to be pitied. They had so few advantages in respect of love. They could say they longed for a kiss from a bouncy wife in a vicarage garden. They couldn’t say she roared under me and clutched my back, and I shot my specimen to blazes.

ROGER MCDONALD, Mr. Darwin’s Shooter

The best place to begin a reassessment of our conflicted relationship with sexuality may be with Charles Darwin himself. Darwin’s brilliant work inadvertently lent an enduring scientific patina to what is essentially anti-erotic bias. Despite his genius, what Darwin didn’t know about sex could fill volumes. This is one of them.

On the Origin of Species was published in 1859, a time when little was known about human life before the classical era. Prehistory, the period we define as the 200,000 or so years when anatomically modern people lived without agriculture and writing, was a blank slate theorists could fill only with conjecture. Until Darwin and others began to loosen the link between religious doctrine and scientific truth, guesses about the distant past were restricted by church teachings. The study of primates was in its infancy. Given the scientific data Darwin never saw, it’s not surprising that this great thinker’s blind spots can be as illuminating as his insights.

For example, Darwin’s ready acceptance of Thomas Hobbes’s still-famous characterization of prehistoric human life as having been “solitary, poor, nasty, brutish, and short” left these mistaken assumptions embedded in present-day theories of human sexuality. Asked to imagine prehistoric human sex, most of us conjure the hackneyed image of the caveman dragging a dazed woman by her hair with one hand, a club in the other. As we’ll see, this image of prehistoric human life is mistaken in every one of its Hobbesian details. Similarly, Darwin incorporated Thomas Malthus’s unsubstantiated theories about the distant past into his own theorizing, leading him to dramatic overestimations of early human suffering (and thus, of the comparative superiority of Victorian life). These pivotal misunderstandings persist in many contemporary evolutionary scenarios.

Though he certainly didn’t originate this narrative of the interminable tango between randy male and choosy female, Darwin beat the drum for its supposed “naturalness” and inevitability. He wrote passages like, “The female . with the rarest exception, is less eager than the male ... [She] requires to be courted; she is coy, and may often be seen endeavoring for a long time to escape the male.” While this female reticence is a key feature in the mating systems of many mammals, it isn’t particularly applicable to human beings or, for that matter, the primates most closely related to us.

In light of the philandering he saw going on around him, Darwin wondered whether early humans might have been polygynists (one male mating with several females), writing, “Judging from the social habits of man as he now exists, and from most savages being polygamists, the most probable view is that primeval man aboriginally lived in small communities, each with as many wives as he could support and obtain, whom he would have jealously guarded against all other men [emphasis added].”4

Evolutionary psychologist Steven Pinker appears to be “judging from the social habits of man as he now exists” as well (though without Darwin’s self-awareness) when he bluntly asserts, “In all societies, sex is at least somewhat ‘dirty.’ It is conducted in private, pondered obsessively, regulated by custom and taboo, the subject of gossip and teasing, and a trigger for jealous rage.” We’ll show that while sex is indeed “regulated by custom and taboo,” there are multiple exceptions to every other element of Pinker’s overconfident declaration.

Like all of us, Darwin incorporated his own personal experience—or its absence—into his assumptions about the nature of all human life. In The French Lieutenant’s Woman, John Fowles gives a sense of the sexual hypocrisy that characterized Darwin’s world. Nineteenth-century England, writes Fowles, was “an age where woman was sacred; and where you could buy a thirteen-year-old girl for a few pounds—a few shillings, if you wanted her for only an hour or two.. Where the female body had never been so hidden from view; and where every sculptor was judged by his ability to carve naked women.. Where it was universally maintained that women do not have ornasms; and yet every prostitute was taught to simulate them.”

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