This week, I want to look at recent discoveries in one of my favorite subjects — sex. Discoveries that reveal surprising male subtlety. Discoveries that could, perhaps, have implications for how we approach in vitro fertilization (I.V.F.).

First: meet the meadow vole, Microtus pennsylvanicus, a small rodent that lives in North America. When a male copulates, the number of sperm he gives his mate depends on circumstances. If he smells other males in the neighborhood, he ejaculates more sperm than if he doesn’t.

Or consider the earthworm Eisenia andrei. These are hermaphrodites: they have both male and female parts. Earthworms aren’t known for their sophistication, yet these animals, too, tailor their ejaculates for different occasions. An earthworm mating with a worm that has had sex before gives around three times more sperm than it does when mating with a virgin. (Sex in hermaphrodites can take one of two forms, depending on the species. Either one partner plays the male and the other plays the female; then they — usually — swap. Or both animals transfer sperm to each other simultaneously. These earthworms are of the simultaneous type, so an animal will lose both virginities in the same sexual encounter.) How can worms tell if their partners have mated before? It’s not clear; perhaps virgins smell different from other worms.

Why does this happen? If more than one male copulates with the same female, then sperm from the different males may compete within her reproductive tract to fertilize her eggs — a phenomenon known as sperm competition. If sperm competition is like a raffle — the more tickets you buy the more likely you are to win — then the male who provides the larger number of sperm will have a better chance of fertilizing her eggs.

A caveat: the chance of sperm competition depends not only on how females behave, but also on their anatomy. In many species, females store sperm, sometimes for years. Here, sperm competition may occur whenever females mate with more than one male. In others — such as humans — females do not store sperm. (Just as well: it would be annoying to suddenly become pregnant 20 years after an event you’ve entirely forgotten.) For species such as ourselves, sperm competition can only happen if a female copulates with more than one male while she is fertile.

The risk of sperm competition has long been known to drive the evolution of the number of sperm that males produce. In species where females routinely mate with more than one male, males have evolved to make more sperm than in those where females are prim. What has only recently been discovered is that males in many species make subtle alterations to their ejaculates on a copulation-by-copulation basis, depending on their assessment of immediate sperm competition risk. (This isn’t under conscious control; the male’s body just does it.) For it’s not just meadow voles and earthworms. Male fowl alter their ejaculates depending on a variety of factors, including their own social status and the presence of rivals. Male Australian field crickets give virgins inferior ejaculates — ejaculates with fewer live sperm — than they give a female who has mated once before. The list goes on.

Which raises the question: If all these other males have evolved to alter their ejaculates with the circumstances — what about humans?

The short answer is: we don’t know. Questions about human sex are often difficult to answer, because the experiments are hard to conduct — there are practical and ethical problems. However, a couple of lines of evidence suggest human males may be no different from the others.

First, there’s the matter of sperm competition. The extent to which this has been a force in human evolution is controversial, because of what it says about the sexual behavior of our female ancestors. As I mentioned a moment ago, sperm competition can only happen in humans if a woman has sex with more than one male during the time when she is fertile. This means that she has to have sex with at least two men in the same week. (The exact window of opportunity is the subject of debate; but although the egg is only viable for about 24 hours, sperm can survive in the reproductive tract for at least a few days.)

This certainly happens occasionally. There are a handful of reported cases of non-identical twins having different fathers — which can only happen if a woman ovulates two eggs at once (which happens from time to time) and also has sex with two men. The question is whether sperm competition happened often enough in our past to have shaped the sexual physiology of men.

The odds are that it did. A standard indicator of the risk of sperm competition is the ratio between a male’s body size and his testes: the larger the relative size of the testes, the greater the historical risk of sperm competition. (Larger testes mean larger numbers of sperm.) Chimpanzees — a species in which females are fantastically promiscuous — have enormous testes. Gorillas — a species where they’re not — have tiny testes. Humans are in between, albeit closer to gorillas than to chimps — which is consistent with a moderate, but not huge, risk of sperm competition in the past. So, do men tailor their ejaculates depending on how they perceive the risk of sperm competition from one situation to the next?

Possibly. It seems that the quality of the ejaculate a man produces by masturbating can be altered by having him look at sexual videos and images while he does so. Men — even those with vanishingly low sperm counts — ejaculate more healthy sperm if they masturbate while watching sexual videos than if they do it while staring at the ceiling. And the effect doesn’t stop there. Men shown explicit pictures of a woman with two men (potential rivals) produce a higher proportion of swimming sperm than men shown explicit pictures of three women.

Whether this translates to sex under different circumstances is unknown. But it does raise an interesting practical consideration. Ejaculates produced during masturbation are often used for I.V.F. Manipulating the stimuli a man watches while making his contribution might substantially improve the quality of what he provides.

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NOTES:

For ejaculate adjustment in meadow voles, see delBarco-Trillo, J. and Ferkin, M. H. 2004. “Male mammals respond to a risk of sperm competition conveyed by odours of conspecific males.” Nature 431: 446-449. In earthworms, see Velando, A., Eiroa, J., and Domínguez, J. 2008. “Brainless but not clueless: earthworms boost their ejaculates when they detect fecund non-virgin partners.”

The classic paper on sperm competition is: Parker G. A. 1970. “Sperm competition and its evolutionary consequences in the insects.” Biological Reviews 45:525-567. For sperm competition driving the evolution of sperm numbers, see Parker G. A. 1990. “Sperm competition games: raffles and roles.” Proceedings of the Royal Society of London B 242:120-126. For ejaculation adjustments in fowl (Gallus gallus), see Pizzari, T., Cornwallis, C. K., Løvlie, H., Jakobsson, S. and Birkhead, T. R. 2003. “Sophisticated sperm allocation in male fowl.” Nature 426: 70-74. In Australian field crickets (Teleogryllus oceanicus), see Thomas, M. L. and Simmons, L. W. 2007. “Male crickets adjust the viability of their sperm in response to female mating status.” American Naturalist 170: 190-195.

For a review of the controversies over sperm competition in humans, and a consideration of the evidence, see Shackelford, T. K., Pound, N. and Goetz, A. T. 2005. “Psychological and physiological adaptations to sperm competition in humans.” Review of General Psychology 9: 228-248. For cases of twins with different fathers, see Phelan M. C., Pellock J. M., and Nance W. E. 1982. “Discordant expression of fetal hydantoin syndrome in heteropaternal dizygotic twins.” New England Journal of Medicine 307:99-101. For a comparison of humans with gorillas and chimpanzees, see Short R. V. 1979. “Sexual selection and its component parts, somatic and genital selection, as illustrated by man and the great apes.” Advances in the Study of Behavior 9:131-158.

For videos affecting ejaculate composition in humans, see Yamamoto, Y., Sofikitis, N., Mio, Y., and Miyagawa, I. 2000. “Influence of sexual stimulation on sperm parameters in semen samples collected via masturbation from normozoospermic men or cryptozoospermic men participating in an assisted reproduction programme.” Andrologia 32: 131–138. For image content affecting ejaculate composition, see Kilgallon, S. J. and Simmons, L. W. 2005. “Image content influences men’s semen quality.” Biology Letters 1: 253-255.