March 27, 2002

Kissing cousin or close kin? One sniff is all some animals need to tell difference, Cornell behavior researcher discovers

ITHACA, N.Y. -- The tiny Belding's ground squirrels appear to be "kissing."

Instead, they are sniffing to analyze secretions from facial scent glands, hoping to learn from the complex odor bouquet who is family and who's not. More remarkably, they are determining in a matter of seconds precisely who is close-enough kin to risk their lives helping -- and perhaps even whether they are too closely related to for mating.

"It's as if these squirrels are reading DNA fingerprints and drawing the family tree with their noses," says Cornell University psychology researcher Jill M. Mateo. Her five years of field studies in the California mountains, as reported in the Proceedings: Biological Sciences (April 7), a journal of The Royal Society, Britain's national academy of science, are the first to show how recognition odors allow precise estimates of kinship, even among distant relatives.

Published as "Kin-recognition abilities and nepotism as a function of sociality" and funded by the National Science Foundation, the study examines potentially risky nepotistic behaviors that are shown to close relatives. It aims to answer the questions: How do social animals, such as Belding's ground squirrels, determine which other animals have a genome so similar to theirs that helping them survive is like perpetuating one's own complement of genes? And how do they know where to draw the line, declining to help more distant relatives because, even though they smell vaguely similar, the genetic benefits of helping do not outweigh the costs of help?

The psychologist is reluctant to extend the squirrel behavioral studies to human affairs. Yet she is mindful of experiments by others, including studies of human odors, which suggest that kin-recognition by smell evolved across a wide variety of animals. So far, Belding's ground squirrels are the champions of kin-sniffing, but many more species remain to be investigated.

"The word nepotism originally meant favoritism shown to nephews, but that's further than these ground squirrels will go. Nepotism in Belding's ground squirrels is limited to mothers, sisters and daughters. Nieces, nephews and more distant kin can be sensed in considerable detail but they are treated like outsiders," Mateo says. She describes the risks and benefits of nepotism in a squirrel world where territorial defense and predator-avoidance often spell the difference between finding the next meal or becoming one:

o Because male Belding's squirrels leave their natal territory after weaning, colonies of burrows are inhabited by related females of various ages (and a few young males that have yet to leave).

o Cooperative territorial defense is important to preserve nest sites and to keep infanticidal adults away from vulnerable young, but fighting can cost injuries or even lives. Risking life and limb for distant kin or unrelated animals doesn't make evolutionary sense.

o Sounding the alarm when a predator approaches is even more risky, making a helpful squirrel the first target of a coyote, for example, while the others run for cover. Belding's ground squirrels are more likely to give the alarm if they can help close kin (even if they are eaten, nearly identical copies of their genes are hiding in nearby holes) but they need a precise measurement of relatedness to weigh the benefits of risky behavior.

Previously published studies by Mateo and another Cornell psychologist, Robert E. Johnston, had shown how hamsters use their abilities for "self-referent phenotype matching" (also known as the "armpit effect") to compare other animals' odors to their own and to distinguish strangers from unfamiliar kin. This time she hoped to show that a different species (Spermophilus beldingi ) can "read" the chemical code of the familial scent with unprecedented precision.

Convening a squirrel family reunion in the California mountains would have been too complicated and unscientific ---- although Mateo knew exactly who was related to whom from years of placing identity tags on each new litter -- so she did the next best thing. Without harming the squirrels, she took a wide variety of scent-gland samples, transferred the scents to coded plastic cubes, and placed the cubes at the entrances of individual burrows. Mateo made sure all the odors were new to the squirrels that would smell them, so the animals could not use prior experience to evaluate the odors.

Then she waited for curious squirrels to emerge from their burrows -- and to sniff. If a squirrel spent a long time analyzing the presented scent, that would mean it had detected a less-related or totally foreign odor compound -- in keeping with a well-established standard in olfactory behavior studies. A quick sniff would be all a squirrel needed to recognize the smell of very close kin.

And that's what happened, with a few exceptions. For the most part, scents the squirrels spent the most time sniffing turned out to have come from distantly related or unrelated squirrels. The scents they recognized immediately had come from very close kin, the ones they should be helping to defend territories or evade predators. The more distant the relationships and the greater the differences in genetic make-ups, the more time was spent sniffing and evaluating scent compounds. "The sensitivity and discrimination of their olfactory apparatus is astounding," Mateo said. "They're like furry gas chromatography machines."

The squirrels' precision in kin recognition also suggests another use for scent-based discrimination, the Cornell psychologist says. Animals that tend to avoid incestuous mating with close kin (and the increased likelihood of inheriting gene-related disorders ) might analyze odors to determine whether a prospective mate is a cousin, a kissing cousin or somewhere in between. In a parallel study, also reported in the Proceedings article, Mateo found equally impressive abilities to recognize kin by odor in a non-nepotistic species, the golden-mantled ground squirrel (S. lateralis ). If the golden-mantled squirrels don't use the ability for nepotism, she wonders, might it help them avoid inbreeding in mate choice?

"When other investigators conducted scent studies and asked women to sniff T-shirts that had been worn by men either genetically similar or dissimilar to them, most women preferred the shirts worn by men with dissimilar genes," Mateo notes. "We should not be surprised to find kin-recognition abilities in a cross section of species, including humans."