Beware of Crickets Bearing Gifts

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The insects scandalously embracing in this picture are decorated crickets (Grylllodes sigillatus), which can be found in the southwestern United States, among other places. The droplet on the male’s tail is–for want of a better word–a gift. After producing this glob he sticks it onto the package of sperm he places on the female. After the crickets are finished with their encounter, the female will grab the gift and snack on it.

In an age when penguins can become role models for traditional family values, some people may be tempted to celebrate the decorated cricket as everything a gentleman should be. But before anyone gets carried off on the vapors of chivalry, it pays to take a closer look at those gifts.

Biologists have puzzled over gifts for many years. Decorated crickets are far from the only animals who give them–many species (particularly insects and spiders) are gift-givers as well. Given the effort that males put into giving gifts, there must be some advantage to them. Otherwise, giftless males would be much more successful at reproducing, wiping away the genes that are associated with presenting gifts.

Scientists who study gifts generally agree that the evolution is driven by how animals mate. In many species, females appear to have some control over which males will successfully fertilize their eggs. It may pay for females to make these sorts of judgments, since some males may have genes that will help her offspring survive. In crickets, female choice can be a pretty simple procedure. Once a male cricket places a sperm package on the female, the sperm then make their way into her reproductive tract. Female crickets can cut down the chances that a male will fertilize her eggs simply by plucking the sperm package off her body. On the other hand, females can boost the odds by leaving the sperm package alone, or mating several times with the same male.

As females evolve the power to choose, natural selection may favor males that can influence their choices. And gift-giving, it turns out, is one way to do just that. The bigger a male’s gift, the more likely his sperm will be the one that gets to fertilize a female’s eggs. Some scientists have suggested that big gifts sway females because they must contain nutrients or some other important benefit. Females who prefer bigger gifts get more energy and can have more offspring than females who don’t.

But the timing of cricket courtship is all wrong for this explanation. Males give their gifts to females before they mate, and female make their choice among which sperm to use afterwards. Some scientists have proposed an alternative explanation for the gifts: they are a way that males can manipulate females to produce more of their own offspring.

This idea emerged from research in the late 1990s on fruit flies. Even after sperm have entered a female fruit fly’s body, she can influence which male will become the father of her eggs. Brett Holland and William Rice demonstrated that male fruit flies respond by injecting chemicals along with their sperm that act like antiaphrodisiacs, making it less likely that females will mate again soon.

While this injection made it more likely males would father flies, it has nasty side-effects on the females. Females who get more of these toxins die sooner than others. Females in turn have evolve resistance to these toxic chemicals. While it’s hard to see this tug-of-war in a normal population of flies, Holland and Rice figured out experiments to uncover it. In one experiment, they bred flies so that they only mated monogamously. That got rid of the competition between males, and their injections became less toxic. At the same time, the females in the experiment lost their resistance. In essence, Holland and Rice figured out how to run the arms race between the sexes in reverse.

Scott Sakaluk of Illinois State University and his colleagues wondered if decorated crickets also followed this "chase-away model" of sexual selection. Perhaps the gifts somehow interfered with female choice. The females ate them not because they were valuable food, but because they were just deceptively attractive. And perhaps the females had evolved to resist the gifts, in ways that might be hard to see from ordinary encounters between decorated crickets.

Scientists have done only a little research on the chemistry of the gifts, but what they’ve found out certainly supports the chase-away model. The gifts contain a lot of free amino acids, which give off an odor that insects may use to recognize good food. But the gifts turn out to have very few of the kinds of amino acids that are actually essential for an insect’s survival. It’s cricket junk food–engineered through evolution to exploit a "sensory bias" as it’s known in the females.

Sakaluk hypothesized that male crickets were taking advantage of the sensory bias of females to give their sperm more time to fertilize their eggs. The longer a female spends eating a gift, the longer it take for her to remove the sperm package from her body. Sakaluk came up with a way to see test this idea. Comparisons of crickets show that originally they produced sperm packages but no gifts. The gifts evolved later, and only in certain cricket lineages. Sakaluk reasoned that female crickets from gift-less species should have a pre-existing weakness for gifts. So he fed the decorated cricket gifts to females of three other cricket species as they were courting. They eagerly feasted on the gift, and the males who mated with them were able to get twice as much sperm into them than without a gift. (His work will appear in the January 2006 issue of American Naturalist.)

The gifts are apparently more than just a tasty distraction, however. The males apparently spike them with an antiaphrodisiac. Sakaluk found that when female crickets of other species at the gifts, they were much slower to mate again. Without a gift, 82% of female house crickets in his experiment mated again within a day. But only 43% of females who ate a decorated cricket gift did.

Gifts allow males to manipulate females to their advantage. But their manipulation puts a female at a distinct disadvantage. Sakaluk has found that the more males a female decorated cricket can mate with, the more offspring she produces that survive to maturity. That would suggest that mutations that allow females to resist the effects of gifts may be favored by natural selection. And Sakaluk has found evidence that this resistance has indeed evolved. Unlike other species, a female decorated cricket can eat a gift and not experience any delay in finding her next mate. Sakaluk proposes that when male decorated crickets first began delivering antiaphrodisiacs, the females were as vulnerable as other species are today. But since then they’ve built up so much resistance that the chemicals have no effect on them.

Can we see a reflection of our own lives in the decorated crickets? Not when it comes to gift giving, no matter how cynical you may be about why men give women roses or chocolates. But men and women do have some conflicts of interest when it comes to children. The faster a baby grows in her mother’s body, for example, the healthier it will be in later life. But if it grows too quickly, the mother may suffer and ultimately have fewer babies. Some evidence suggests that our genes have been shaped by this conflict. Male versions of certain genes spur babies to grow faster, while the female versions slow them down.

Even leaving our own evolution aside, Sakaluk’s research is fascinating. It’s part of a burgeoning field of research that you can read about in the new book, Sexual Conflict. The crickets in your backyard are locked in an arms race that began long before we came on the scene, and will continue long after we’re gone.