And God said, ‘Let the waters bring forth swarms of living creatures, and let birds fly above the earth across the firmament of the heavens.’ So God created the great sea monsters and every living creature that moves… And God saw that it was good. And god blessed them, saying, ‘Be fruitful and multiply and fill the waters of the seas, and let birds multiply on the earth.” (Genesis 1:20-22) This is the first great commandment, and it so important to have sex that it is repeated no less than seven times in the first book of the Bible.
Have plenty of sex, yes—but God does not say how! Until recently, we thought that Darwin was right—that there was only one way to have sex. The English philosopher Herbert Spencer summarized the great biologist’s thesis in the memorable phrase we all know, “the survival of the fittest.” In his The Descent of Man, 1871, when evaluating his phrase “the struggle for existence,” Darwin wrote: “The expression used by Mr. Herbert Spencer, ‘Survival of the Fittest,’ is more accurate.”
So up until the 1970s, it was scientific dogma that the males in every species of dung beetles and damselflies alike, all wanted to grow up to be fighters. That is, they wanted to acquire and defend territories and harems. At least in theory, the combined forces of natural selection (getting killed by rivals or chosen by females) would ruthlessly out any sissy alternative lifestyles. In fact, Charles Darwin himself noticed that alternative forms persist in many species. But biologists generally ignored this insight because they couldn’t explain it or they just didn’t see it in the first place. Sneaky behaviors designed to fool other members of the same species often fooled outside observers too.
A mate might actually benefit from being smarter, weaker and, well, more effeminate. For instance, in bluegill sunfish a significant percentage of males actually impersonate females. They wear female striping and their eyes darken to resemble the limpid pools of a female bluegill. They also have heightened levels of the female hormone estradiol. The phrase “satellite males” describes the way these impersonators orbit the nests of conventional males.
Conventional males frequently get fooled and invite the cross-dressers into their nests. In entering a nest a female impersonator dips down and turns on one side, moving as a real female would to release eggs for the resident male to fertilize. But the cross-dresser is in fact secretly releasing his own sperm onto the eggs deposited by females.
This kind of transvestite mating tactic has turned out to be surprisingly common in other species. Take the giant cuttlefish, a voluptuous, three-foot-long relative of the squid. Conventional mates are the Beau Brummells of the marine world. They put on a lavish, romantic display for the females. A courting male waves extended, banner-like webs and arms, and turns his body into an amorous light show with bright colors and pulsing zebra stripes. So far, so good. But sometimes a small sneaker mate accompanies the happy couple and, by assuming the shape and body patterns of a female, avoids attack. Sooner or later, the macho males will have to drive off some other big mate. In the resulting confusion: the female impersonator waltzes in, sneaks under the covers, grabs the female and starts passing sperm to her. When the macho mate comes back, the sneaker male once again tags along, looking girlish and innocent.
Cross-dressing isn’t just a way to get a mate. Some female damselflies, for example, appear to imitate males for the opposite reason—to avoid being sexually harassed. Most of the time, though, cross-dressing and other sneaky ploys have just one purpose: getting the girl. This is why the big boys of the world spend so much time and energy on what biologists call “mate guarding.”
The dung beetle, for instance, regularly patrols his tunnel to check on the female, and if he catches her having sex with another dung beetle who has sneaked in behind his back, he throws the interloper out. Then he immediately has sex with the female beetle to displace the interloper’s sperm with his one. In fact, he may have sex with her ten times a day, just to be certain—or at least a little less certain—that he’s the father of her offspring. Water bugs are even more anxious about paternity. In one study, a male mated with the female 100 times in 36 hours! The burden of mate guarding, whether by fighting or marathon lovemaking , can leave even the sturdiest male feeling weak-kneed.
Among northern elephant seals, a bull who wins bloody contests against other bulls gets to stake out a beach and wallow in splendor as king of his harem. He may mate with five females in a season, while many lesser males go celibate. But defending his harem also means not going back to the sea to eat, and he typically loses about four percent of his weight during the three-month breeding season.
This is why “success” as a conventional male is not always all it’s cracked up to be. DNA testing in red-winged blackbirds, for instance, has revealed that the longer a resident mate stays away from the nest gathering food, the greater the likelihood that his putative offspring will actually be fathered by someone else. In one Australian bird species, the fairy wren, fully two-thirds of the offspring get fathered by someone other than the man of the house. If male animals could perform a cost-benefit analysis, they would almost certainly conclude that it’s cheaper and easier to be a sneaker male. You don’t have to keep up a large territory, court females, fight off rivals or provide parental care.
But is cheaper ever really better? In most species, females are the choosers when it comes to mating, and they usually seem to prefer the big boys. Northern elephant seal females, for instance, clearly regard the big beefy bull as their best possible mate. They howl in protest when the bull mounts them—but they howl louder and longer if a lesser male tries it, so the big bull will come thundering to the rescue.
Still, the strategy that’s lord of the dancer one season may be just a spectator the next. Take the side-blotched lizards living among rocky outcrops in the coastal mountains of central California. They’re about two and a half inches long, and conventional males typically display by doing push-ups while also puffing out the bright patch of color at their throats. Here we see three different, genetically determined mating tactics, with each identified by a distinctive throat color.
The orange-throats are the “ultra-dominants,” patrolling large territories with lots of females. The blue-throats are about 15 percent smaller, but still manage to maintain modest territories and diligently mate-guard as many females as they can round up. And then there are the yellow-throats, which mimic females, do no push-ups and maintain no territories, but instead skulk in nooks and crannies among the rocks hoping to get Lucky. It ought to be easy for everyone to spot the slackers and make them disappear.
But is life that simple? If the blue-throats happen to predominate in the population, then the slacker yellows are indeed out of luck. The blue-throats recognize them as rival mates and evict them from their territories. But blue-throats never predominate for long, because the dominant orange-throats have the size and stamina to beat them up and take away their females. Thus orange-throats get more offspring in the next generation, and in a year or two they supplant the blues.
But orange-throats apparently are not so bright. They don’t recognize the slacker yellow boys as rival males, so they tolerate them in the neighborhood. This allows the yellows to make “little sperm strafing runs” through orange-throat territories. “After a year or two,” yellow slackers actually outnumber orange-throats. Then it’s time once again for the blue-throats to make their move. In fact, the three male types regularly displace one another in the reproductive hierarchy every four-five-year cycle.
In many other species, the sneaky approach seems to work best when picky females concentrate their favors on a relative handful of big brutish males (or when the big brutes corral females in harems. The macho-males do best with this kind of strong sexual selection, but the overwhelming majority of conventional males wind up as losers. So sneaker mates in this scenario may actually do better on average than the ordinary ones. “Any time you have a great imbalance between the haves and have-nots,” says Purdue University biologist Richard Howard, “the have-nots find a way around.” Sneaking also works in habitats with lots of places to hide when the big guy comes on the scene.
So what does all this mean for us humans? The mating strategies of people are at least as diverse as those being studied in the rest of the animal kingdom. Since humans are part of the vast web of life, why should we be singled out by, say, the Church or politicians, and told that the Lord ordained only one way to have sex. Why can’t we legally enjoy the same flexibility in our mating strategies that our living associates have? After all, even though the Lord told us “to be fruitful and multiply,” he didn’t specify as to how!