VIKING ADULT, MAY 2014It’s early spring in the Adulam Grove Nature Reserve near Jerusalem. On the rocky ground, among fallen prickly oak leaves, scurry some woodlouse-hunting spiders. One female turns a corner and suddenly feels the legs of a waiting male tap her backside. The next thing she knows, she is grabbed and incapacitated by his powerful jaws while he has his way with her.

Sexual congress in the aptly named Harpactea sadistica is anything but gentle. The male turns his mate upside-down and forcefully pushes his needle-like palps six, seven times through the skin of her belly. As in all spiders, H. sadistica’s palps serve as his genitals, and with each puncture he injects sperm into her. The sperm cells swim autonomously through her body, finding and fertilizing her eggs without any need for copulation, vagina, or oviduct.

So-called traumatic insemination of this sort occurs...

In The Descent of Man, and Selection in Relation to Sex, Charles Darwin noted that the “strong passions” of male animals cause them to “eagerly pursue the females.” The latter sex, on the other hand, are “coy,” and seen “endeavouring . . . to escape from the male.” In other words, males tend to compete for access to the females’ eggs, and females typically choose their suitors prudently. Hence magnificent mandrills, gaudy grouse, and sweet-voiced cicadas—a kaleidoscopic cornucopia of form shaped by female choice.

Only in 1948 did science elucidate the Darwinian benefits that males reap from their strong passions. English geneticist Angus Bateman’s experiments showed that for male fruit flies, more copulations mean more offspring. For females, however, additional matings beyond the first one usually don’t pay off. Then, in 1972, sociobiologist Robert Trivers of Rutgers University reasoned that this discrepancy was all about parental investment; if males contribute only tiny sperm, whereas females invest gestational space, time, and resources, then males will evolve to be super-wanton, and females will be hyper-choosy. Hence H. sadistica’s traumatic insemination, where the male and his genitalia have evolved strategies to subvert the female’s choosiness.

But Trivers also made biologists realize that sex roles need not be fixed—they can even be reversed. (See “The Hidden Side of Sex,” page 28.) If males evolve to “donate” more and more sperm to a female, either to outcompete other males or to counter a female’s tendency to “dump” or digest most of his sperm without giving it access to her eggs, the balance of parental investment shifts towards the males. At some point, the male may be producing so much semen that it can no longer be seen as cheap. Mormon crickets, for example, produce huge sperm packets that weigh a quarter of their own body weight, which nutrient-starved females are keen to devour—making them eager pursuers of the males.

It’s the same in some insects in which the male penis has become reduced and instead the female has evolved an intromittent organ to gain access to his spermatophores. For example, when Brazilian Neotrogla cave lice mate, the female sits on top of the male, inserts her mace-like she-penis into his nether region, and uses it to suck up the sperm package that costs the male so much to make.

Individual sperm cells may also gain weight: in some crustaceans and insects, the males produce giant sperm that are up to ten times as long as their own body, and approach the weight of an egg. Their genitalia are adapted to coping with such complicated ejaculates. Some freshwater crustaceans are blessed with a mechanical-looking ejaculation tube, lined with a series of cogwheel-like flanges that pump the huge sperm cells, one by one, into the female.

Such surprises drive home the point that sexual selection is really not about males and females. It’s about which sex has the most to gain from a mating. Depending on where the balance lies, sexual selection molds males, females, or both. And this leads to such mind-boggling wonders as traumatic insemination in the semideserts of the Near East and, as if to even the score, female rape of male cave lice in Brazil

Menno Schilthuizen is a research scientist at Naturalis Biodiversity Center in Leiden, the Netherlands, and a professor of character evolution at Leiden University. You can read an excerpt from Nature’s Nether Regions: What the Sex Lives of Bugs, Birds, and Beasts Tell Us About Evolution, Biodiversity, and Ourselves.

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