Female Choice Continued After Copulation Began

The role of female choice in penis evolution is revealed in the way the penis is used during copulation. Biologist William Eberhard has argued that copulation is not the end of courtship, but rather its most intense phase. In most species, female choice does not end when a male penis first enters, but can continue until sperm actually reach a fertile egg. Eberhard calls this "copulatory courtship." Some female insects can store the sperm of several males for weeks and use it when they want to fertilize their eggs. Many female mammals (unconsciously) squeeze the ejaculate of some males back out after copulation—a process called "flowback"—as if rejecting sperm from males whose copulation is not up to their standard. In a human female with concealed ovulation, a male's sexual ability may influence whether she keeps copulating with him, and that will determine his likelihood of producing offspring with her. If she rejected him after one or two unexciting encounters, he is very unlikely to father her children.

The duration and intensity of copulatory courtship in a species is a clue to the power of female choice. If efficient sperm delivery were the only point of copulation, a single thrust would be sufficient. Tomcats use this hit-and-run strategy. Copulation in most birds is very brief, and this absence of copulatory courtship is probably why birds have not evolved penises. Most primates make several separate "mounts" and several thrusts per mount before ejaculating. Copulatory thrusting seems designed to maximize the intensity, duration, and rhythmicity of tactile stimulation delivered to the female genitals. Delivering stimulation in addition to delivering sperm suggests that female choice has been important.

Copulatory courtship was probably especially important among hominids. Continuous sexual receptivity and concealed ovulation gave our female ancestors an unprecedented opportunity for testing males as sexual partners, while running a lower risk per copulation of unwanted pregnancy than any other primate did. Sex during menstruation, pregnancy, and breast-feeding would also have given ample opportunity for judging potential long-term lovers by their copulatory skills.

In species that do not use copulatory thrusting, especially insects, penises evolve more obvious tactile stimulators: nubs, spikes, ridges, curls, barbs, hooks, and flagella. Male insects often try to push each other off during copulation, so copulatory thrusting would risk disengagement. Better to lock the genitals together and have internal flagella to excite the female. With primates, it is not so common for male rivals to swarm over females knocking each other off. This allows couples a bit more copulatory leisure, with more complex movements favoring simpler penis designs. The human penis is especially streamlined because ancestral females apparently favored whole-body copulatory movement over the flagellar vibrations favored by female insects. Perhaps whole-body copulatory movements, requiring much more energy than waving a couple of vibrators on the end of the glans, were better indicators of physical fitness. It is not clear whether many middle-aged men do actually have heart attacks during vigorous sex with mistresses, but this plausible risk reveals the energetic costs of human copulation, and one way that female demands for tactile stimulation separate the healthy from the unhealthy. The loss of the baculum (penis bone) also reveals female choice for tactile stimulation. Since male human penises become erect with blood rather than muscle and bone, this gives them more flexibility, and permits a greater range of copulatory positions. Although bonobos also enjoy face-to-face copulation, their positional variety pales in comparison to the Kama sutra. Human penises evolved as tactile stimulators for use in copulatory courtship. Further research may clarify whether penises and copulatory courtship evolved mostly as fitness indicators or just as sexually selected entertainment.

Female hominids may not have preferred thicker, longer, more flexible penises per se. They may simply have liked orgasms, and larger penises led to better orgasms by permitting more varied, exciting, and intimate copulatory positions. This rather contradicts the view of the penis as a symbol of male domination. If we were a species in which males dominated the sexual system, we would have one-inch penises like dominant gorillas. The large male penis is a product of female choice in evolution. If it were not, males would never have bothered to evolve such a large, floppy, blood-hungry organ. Ancestral females made males evolve such penises because they liked them.

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