Primate business

A female study subject (with twins) scent marking at the Duke Lemur Center
David Haring/Duke Lemur Center

Sniffing the armpit of a sweaty T-shirt seems like it would give you more information about a person’s laundry habits than their potential qualities as a mate. But an array of complex signaling chemicals in sweat and other secretions allows humans and other primates to determine just who would make the best partner.

One gleaming orange eye opened, then the other. These eyes, set in tufts of black fur against a gray face, belonged to a male ring-tailed lemur (Lemur catta) and tracked the path of graduate student Jeremy Chase Crawford as he walked by. That day, at the Duke Lemur Center in Durham, North Carolina, Crawford carried with him a set of three wooden dowels.

The primate began jumping when he saw the dowels, and as Crawford came closer, he began making clicking sounds and grunting, signs that he was excited. For the male lemur, the three wooden dowels represented a chance to discover smells from new females he might one day mate with.

Crawford, a PhD student in the lab of social anthropologist Christine Drea, had swabbed two of the dowels with genital secretions from two different female lemurs: one that been injected with Depo-Provera, a contraceptive hormone, to prevent her from mating while housed with sons and brothers in zoo settings, and one that had not received any contraceptives. (The third dowel was a control and had been swabbed with unscented cotton.) Crawford’s experiments are helping to determine if contraception affects how female lemurs smell to others in their troops.

In the indoor testing room at the Duke Lemur Center, Crawford watches a male subject responding to a female’s odor presented on a dowel.
David Haring/Duke Lemur Center

“We’re not aware of olfactory signals on conscious level,” says Cheryl Asa, Director of Research at the Saint Louis Zoo. “We’ve known for a long time that if you change the hormonal profile of the animal, you change a lot of things.” In a recent study, human males rated the sweaty T-shirts of ovulating women as better smelling than those of nonovulating women (Psychological Science, 21:276-83, 2009). By studying lemurs, Crawford and Drea are hoping to tease apart the molecular pathways behind olfactory signaling.

After Crawford placed the three dowels in the lemur’s enclosure, the male approached the one that had been swabbed with the gential secretions from the female treated with Depo-Provera, his long gray-and-black striped tail arched in the air. He rose up slightly on his hind legs, grabbed hold of the dowel with his leathery front paws, and gave it a good sniff. He paused briefly, and then headed over to the next one, where he repeated the process. This time, he didn’t pause before moving on to the final dowel.

The male began sniffing the remaining dowel, and didn’t stop there. He began to lick it as well, right where Crawford had swabbed the genital secretions from the female who hadn’t received contraceptives. This love fest went on for about 10 seconds, and just as the male was about to leave the last dowel, he turned back, gave it one last sniff, and walked away.

Each lemur has a unique odor signature that conveys a variety of information about
its genetic makeup and whether it’s able to breed.

Genital secretions in L. catta contain over 300 unique chemicals, the precise proportions and types varying from animal to animal. Each lemur has a unique odor signature that conveys a variety of information about its genetic makeup and whether it’s able to breed. In the ring-tailed lemur, high heterozygosity signals high genetic quality. This desirable attribute is signaled by a higher proportion of high-molecular-weight fatty acid esters in their genital secretions, and a decreased proportion of volatile fatty acids.

“Contraception,” Crawford says, “messes all of that [signaling] up.” All female lemurs on contraception smell alike. Their unique odor signatures essentially disappear, and males cannot decide which female would be better to court. It would be almost as if a human male had to pick out a mate from a lineup of identical female mannequins. “Contraception eliminates the cues of individual identity,” Drea says.

“We would expect any of the sexual signals to be different [in females on contraceptives], but that it masks other info about individual identity is something unexpected,” Asa says.

All of this matters little to the male lemur when Crawford enters the enclosure to remove the dowels. It squeals in protest as he takes them. After one last desperate grab at the dowels, the lemur lets go and shakes his tail at Crawford in silent protest.

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