in the tanks, but at eleven they darted around the tank as if something was bothering them. After pondering this strange behavior for a time, Tinbergen realized that the timing of the fish agitation coincided with the daily arrival of the mail truck. The fish that exhibited the strange behavior were in a tank by the window in sight of the truck’s arrival, and the truck was bright red.
A stickleback with a reddish tinge is a stickleback spoiling for a fight. Evidently, this red truck was enough to get the sticklebacks in the tank annoyed and ready for a fight. “We’ve tried to eliminate the color red from most things in the stickleback room so that we don’t redo the mail truck experiment,” says David Kingsley, a geneticist at Stanford University. There’s nothing dangerous to a fish about a mail truck, but the general stimulus brings a very specific response, and that’s really interesting.
Kingsley is trying track down the genetic changes that gave us our big brains, our ability to walk upright, and our largely hairless bodies. To understand human evolution, Kingsley has turned to fish. Here is Kingsley’s thinking. New environments allow new forms to appear. That’s part of what Charles Darwin concluded when he studied the beaks of finches on the Galapagos Islands off the coast of Ecuador. Each island has a slightly different ecology, and on each island, the finch beak was uniquely adapted to the ecology of that island. So Kingsley wanted to find a species that had recently—recently, in evolutionary terms—been forced to adapt to new environments. It turned out that the stickleback was ideal.
Sticklebacks are about two or three inches long. They normally live in the ocean but migrate to coastal areas to breed each spring. Fifteen thousand years ago, ocean sticklebacks all looked pretty much the same. Then came the end of the ice age, and glaciers started to recede. That created a number of new streams, lakes, and coastal estuaries, all potential new homes for sticklebacks. Each of these new environments presented challenges. Different colored water and vegetation required different coloration to make it possible for the sticklebacks to avoid detection by predators. The various predators prompted the stickleback to evolve different kinds of body defenses, such as changes in skeletal armor that make the sticklebacks harder to catch. In some places, merely being a larger size was adequate to allow the sticklebacks to thrive.
Kingsley wanted to find the genes that were responsible for all of these changes, because he hoped that they would allow him to track down the kinds of genes that also changed when humans made a similar migration from one fairly homogenous environment to a variety of new environments with new challenges. That migration took place about a hundred thousand years ago, when our ancestors left Africa. As we moved away from the intense sun near the equator, we lost some of our melanin, which had protected our skin from all of that sunlight. Colder climates also resulted in thicker hair and stockier builds. Even our diets changed, requiring new sets of enzymes to help us digest our food.
Kingsley has collected sticklebacks from all over the world, in a variety of shapes and colors. Just as Gregor Mendel crossed pea plants to find genes, Kingsley crossbreeds sticklebacks and tracks the genes he’s interested in through successive generations. He breeds the fish in dozens of thirty-gallon tanks in the basement of the Stanford Medical School.
Nikolaas Tinbergen’s mail truck story sounds like one of those apocryphal tales that’s simply too good to be true. According to Alun Anderson, however, it is true.
Anderson is a science journalist and author, but before he began his journalism career, he earned a Ph.D. in ethology, the study of animal behavior. “I worked in the same laboratory at Oxford as Niko from 1972 to 1976,” says Anderson. “Niko told me that growing up in the Hague, he had loved to bring home sticklebacks from local streams in a jam jar and watch them.”
Around 1934, when Tinbergen was working in the Department of Zoology at Leiden University in Holland, he and a student, Joost ter Pelkwijk, started to wonder about the red color on the three-spined stickleback.
“In springtime, male sticklebacks develop ‘nuptial colors’ of a bright-red belly and throat and defend their territories,” says Anderson. “The male builds a nest inside its territory and will court and guide females, which have a silvery color, toward it. If she enters and lays her eggs, he will follow her and fertilize them. Then he will protect the eggs from marauders (often other sticklebacks) and guard the young.” The sticklebacks would attack any other males that venture into their territory. “Niko had set up aquarium tanks containing sticklebacks alongside the windows in his laboratory at Leiden University,” Anderson says. “In one of them was a single male in nuptial colours. Pelk and Niko both noticed that this male would regularly start a frantic head-down display, holding itself in the peculiar vertical position designed to tell intruders to get out of his territory, even though there was no other male nearby. The attack was aimed toward the window, and it wasn’t long before they figured out that it began whenever the bright-red post van drove past the window on the way to deliver the letters.”
This led Pelkwijk and Tinbergen to do a famous set of experiments showing that you could provoke a stickleback to attack simply by showing it a red object. “These initial experiments by Tinbergen and others led to a whole body of theory on ‘sign stimuli’ and ‘innate releasing mechanisms,’” says Anderson. More recent work suggests that red alone won’t annoy every male, but once one gets annoyed, others may join in the agitation. Perhaps it’s not all that surprising that red agitates a male stickleback. Certainly, red is a color that elicits a kind of annoyance that matadors in Spanish bull rings are professionally familiar with.
Skunk spray that reminds us of rotting food, red mail trucks that remind fish of fighting, fingernails on a chalkboard that remind us of a scream—these annoyances may have something in common. The unpleasantness is linked to aversive responses that have evolved to keep us alive. The annoyances remind us of something we’re programmed to avoid, triggering a strong reaction. They are a case of mistaken identity—we can’t distinguish between the threat and the thing that mimics the threat.
Rachel Herz doesn’t buy the evolutionary theory about skunks. In fact, she thinks we’re born without any smell preferences at all. Herz nicely details her argument in
Take the smell of rotten eggs—it’s hard to imagine not having a gag reflex to that smell, but Herz says that babies show no aversion to the odor. Young children show no preference for the smell of bananas over the smell of poop. Nursing babies have been shown to actually prefer garlic-scented milk. As for skunks, Herz herself likes the smell. She says that her skunk spray predilection comes from an experience she had as a child: she was out on a sunny summer day with her mother, who exclaimed, “Isn’t that smell nice?” when the skunk spray smell wafted through the air. Herz has liked the odor ever since. Eric Block, who specializes in sulfur compounds, has a similarly warm feeling about skunk spray: “I don’t mind it that much because when I smell it, it kind of reminds me of the work that I do.”
In small doses, some thiols are widely pleasing, even to nonchemists. “You can have pleasant-tasting thiols,” says Block. For example, a freshly opened container of coffee smells wonderful, thanks to a particular thiol. “Thiols at very low concentrations, including methanethiol, are actually very important in the taste of wine and the odor of different types of wine. At high concentrations, the perception is skunky or stinky or garbagey or something like that.” For smells, too, it seems that intensity matters.
Detection also matters, says Herz. Not all humans are thought to have the same odor receptors, meaning that not everyone will smell the same scents. This variation in receptors can make people sensitive to certain scents. For example, if the smell of skunks is particularly annoying to you, it may be because you have more receptors that are sensitive to thiols. What might smell moderately strong to one person could make you gag if you have more receptors for that odor. “It has to do with the intensity,” Herz says. “Even your favorite piece of music is aversive if it’s blaring.” Herz says that this is an instance where there are innate differences in response to smell.
Herz argues that judgments about particular smells come less from an inherent like or dislike but more from the context. She has investigated how association affects our perception of a scent. In one particularly memorable study published in the journal
The researchers found that the labels made a big difference between annoying and appetizing. People strongly liked the smell of what they thought was parmesan but were repelled by the same odor when they were
