Birds, bees – even educated fleas do it. But why? Weird insect genitalia is helping unravel the evolutionary benefits of sex. By Wendy Zukerman.

Insects teaching us about the birds and the bees

Blue damsel flies mating.
Blue damsel flies mating.
Credit: Keven Law

One whiff of the corpse and he was hooked. He tracked the scent to a lusty temptress, who had just killed her former lover, and quickly moved towards her. Without a thought for his fallen rival, the two spiders made sweet, sweet love.

Researchers at the University of Pittsburgh recently discovered that female grass spiders are more attractive to future mates if they cannibalise their previous lovers. It sounds deranged, but these cannibalistic femmes also tended to produce more eggs than females that stuck to eating crickets and, luckily for the second-comer, they only dined once.

Surely there is little more intriguing than the sex lives of spiders and insects. The splendour of their trickery and bizarre genitalia seems never-ending. But over the past few decades, watching the intimate moments of critters has helped scientists understand more than just smut. It has illuminated the forces of evolution, what it is to be “male” and “female”, and even why sex exists at all. “This is the sort of thing that everybody seems to be giggling about, but you should take it seriously,” says Menno Schilthuizen, an evolutionary biologist at the Naturalis Biodiversity Centre in the Netherlands.

Earlier this year, Schilthuizen published Nature’s Nether Regions, an exploration of what bug and beast sex can tell us about ourselves. It opens with one “unassailable” fact, “supported by millennia of bathroom graffiti”: humans find genitals endlessly fascinating. Only recently, however, has this fascination been matched by scientific scrutiny.

Nether regions tend to be the most physically distinguishing feature of many species. Much more than a semen syringe, some penises are so elaborate that Schilthuizen compares them to an exploded grandfather clock. Despite centuries of studying the diversity of the animal kingdom, biologists have catalogued these curious organs but rarely questioned the reason for all that garnish.

When Charles Darwin penned his groundbreaking work The Descent of Man in 1871, he first described how competition for mates could drive changes in physical appearance and behaviour. Strong males pairing with “vigorous females” would produce healthier offspring, he wrote, so allowing their particular traits to pass to future generations. Darwin, however, eschewed genitalia when discussing what an advantageous trait might be, preferring to assess colourful bird plumage and deer antlers.

It’s unsurprising given the religious views of the day. “We can’t possibly have expected him to come out talking about genitalia,” says Leigh Simmons, a professor at the University of Western Australia. But, remarkably, it would take more than a century for scientists to seriously investigate these nuts and bolts.

In the 1970s, studies into damsel flies found that females often mated with more than one male, but contrary to popular wisdom regarding playing “second fiddle”, the succeeding male tended to father the offspring. Jonathan Waage, an entomologist then at Brown University, wanted to know how the second male’s sperm usurped the first. He carefully sliced the female damsel flies open, peering into the sperm mass left behind. Surprisingly, females had roughly the same amount of sperm if they had one or two mates. Where was half of the sperm going?

Waage noticed that when the second males had sex they spent more time “undulating” than releasing sperm. Indeed, these were conniving undulations – the flies were removing their rival’s sperm. Close inspection of the damsel flies’ penises revealed they had handy tools to get this job done, including horns and a flexible head, which may “aid in scooping”, wrote Waage. The work, published in Science in 1979, was a breakthrough. It showed for the first time that genitals are not just vehicles to exchange DNA, but are at the heart of evolution’s pressure.

According to Bob Wong of Monash University in Melbourne, before Waage’s work, scientists thought that reproduction was a “harmonious venture” between the sexes. “Then it dawned on us that sexual conflict is rife in the animal kingdom,” he says. In bed bugs, for example, males inseminate females by stabbing their penis basically anywhere in their partners. The ejaculate of some flies and butterflies contains toxic substances that manipulate females to fertilise more eggs, but it also shortens their life span.

Of course, females aren’t taking all this lying down. Sexual conflict often creates an impressive arms race of genitalia, with the sexes trying to “one-up” each other, says Wong. Male rove-beetles, for example, have a long whip-like appendage that threads through the female’s genital tract to insert their sperm package directly. In response, the female has evolved an equally large vagina, ensuring only deft males can fertilise her.

Much of this sexual conflict arises because the reproductive needs of males and females rarely coincide in the animal kingdom. Males tend to want to spread their seed widely, while females are looking for quality. But why did this particular pattern emerge? Why, for example, isn’t there just one gender? If there were, we could mate with everyone.

While hermaphrodites – those with both male and female reproductive organs – do exist in nature, they remain exotic. Evolution has clearly favoured two sexes. Schilthuizen argues that “males” and “females” evolved to prevent a conflict between little units inside cells called organelles. These units make proteins and control cell activity. A cell needs only one type of each organelle. During intercourse, the sex cell of one animal fuses with another to make offspring, so if both cells had the organelles, they would be in competition – effectively warring with each other. Consequently, it was more advantageous to have a large sex cell packed with organelles – known as the female’s egg – and a small sex cell that needed only to carry DNA. Since eggs take more energy to produce, it’s a better bet for females to invest in quality males to fertilise the “expensive” eggs, says Eric Haag at the University of Maryland. While the “cheap” sperm favours a slutty approach.

But it’s not just about sperm and eggs. “It’s about who invests more time and energy in the offspring,” says Schilthuizen. “If the male invests more, you’ll have a reversal of roles.” In April, Kazunori Yoshizawa of Hokkaido University in Sapporo uncovered the ultimate role reversal: a group of insects called Neotrogla, where females have penises and males have vaginas, at least of a sort. These insects are found only in extremely dry caves in Brazil, where food is scarce. Here, the males invest heavily to make nutrient-packed “nuptial gifts” to give to females during sex. According to Yoshizawa, this has created strong sexual competition among females for the food, so they display typically “male” traits, including penises – quite dominating ones, too, with spines that anchor the males into the sexual positions to force the males into sex for days (the longest act detected by the scientists was 71 hours).

In the few species where the investment in offspring is equal, this classic conflict of the sexes evaporates, says Schilthuizen. In humans, for example, making eggs has become almost a negligible burden for females, at least compared with the main investment of caring for offspring for some two decades after they’re born, and that’s a burden the sexes are expected to share.

But the more common sexual conflict exemplifies one of the greatest misconceptions about evolution: it’s not about species. Evolution is driven by individuals, whose only concern is to carry their genes to the next generation. That brings us to “one of the most fundamental puzzles in evolutionary biology”, as Darrell Kemp of Macquarie University in Sydney puts it: why do animals have sex at all? Natural selection should favour those who pass most of their genes into future generations, but sex with another automatically wipes out half their stock. It’s also risky – in some cases, one can get eaten while in the act – and courting uses time and energy. But while there is a tiny minority of species that have done away with intercourse – such as self-cloning Timema stick insects in North America – the advantage of sex must be “profound”, says Kemp.

Studies into critters suggest that mixing genes with a mate increases the chance their offspring will survive over time. Initially, an individual loses half their genes, but mingling their DNA with another may allow the kids to cope with future environments and new diseases that they themselves couldn’t handle. Witness the asexual populations of the New Zealand snail Potamopyrgus antipodarum, which have more parasitic worm infections than sexual populations of the same species.

While there is much to learn from the intimate antics of snails, spiders and insects, Simmons says that to fully understand human behaviour, we will need to more closely study ourselves. The cave-dwelling Neotrogla might give gifts to their partners for sex, but “if you want to understand what a box of chocolates means, you have to understand human courtship”, he says. Romance lives.

This article was first published in the print edition of The Saturday Paper on September 13, 2014 as "Love bug".

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Wendy Zukerman is a science journalist and host of the Science Vs. podcast.

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