Saturday, September 15, 2012

Scent of the Hyena Clan


Photo by Jaime Tanner.

My crooked path to the world of perfume began with an undergraduate interest in animal behavior. In the hills above the U.C. Berkeley campus, at the field station off Grizzly Peak Boulevard, I built a semi-natural habitat to study Merriam’s kangaroo rats and their ability to detect rattlesnakes by smell. Years later my faculty advisor, Professor Steve Glickman, received a grant to study the reproductive biology of hyenas. They have a matriarchal social organization in which females are behaviorally dominant to males. The females also have a pseudo-scrotum and an enlarged clitoris that resembles a penis.

Steve was interested in the hormonal and developmental processes underlying this unusual anatomy and behavior. The grant enabled him to set up a hyena colony at the field station. This took some doing: the city of Berkeley demanded extraordinary security as they were not too keen on the idea of escaped hyenas prowling the streets. He also had to smooth some feathers with the neighbors. Nearby was the recently established Mathematical Sciences Research Institute, home to some serious poindexters. (Last week’s seminar was “Quasi Periodic Orbits: The Case of the Non Linear Schr√∂dinger Equation.”) Math types like to work at night and they were freaked out by the nocturnal vocalizations from the colony—Crocuta crocuta isn’t known as the laughing hyena for nothing. Steve once invited me up to meet the study animals. Their vocalizations are truly unsettling. I was happy to have a stout chain link fence between us.

Kay Holekamp is another Berkeley student who progressed from rodents (in her case a Ph.D. on Belding’s ground squirrel) to smellier topics—scent marking in hyenas. Kay is now a professor of zoology at Michigan State but spends a lot of time studying hyenas at the Masai Mara National Reserve in Kenya. She and two colleagues have just published a paper on the bacterial basis of clan-specific social odors.

Hyenas live in small clans and use scent to mark their territory.
A particularly common and conspicuous chemical signaling behavior among hyenas is ‘pasting,’ a form of scent marking wherein a hyena typically straddles a grass stalk, extrudes its anal scent pouch, and drags the exposed pouch across the top of the stalk, leaving behind a thin layer of secretion, called ‘paste’. Paste is composed of lipid-rich sebum and presumably desquamated epithelial cells, and it is produced by a pair of lobulated sebaceous glands that secrete their products directly into the anal scent pouch.
Yummy! And effective:
The major volatile constituents of paste are fatty acids, esters, hydrocarbons, alcohols and aldehydes. Collectively, they give paste a pungent, sour mulch odor that persists, detectable by the human nose, for more than a month after paste is deposited on grass stalks.
Scent glands are “warm, moist, organic-rich and largely anaerobic,” and thus “highly conducive to the proliferation of fermentative symbiotic bacteria.” The fermentation hypothesis for chemical recognition holds that:
as bacteria ferment the protein and lipid-rich substrates in scent glands, they produce odorous metabolites that are co-opted by their mammalian hosts as components of chemical signals.
In other words, the deal works like this: the hyena provides a warm, moist, nutrient-rich habitat for the bacteria which in return produce a stinky brew of by-products useful in scent marking.

A corollary of the fermentation hypothesis is that species differences in the hosted bacteria could account for odor differences between individuals or groups. Having identified four separate hyena clans at the Kenyan reserve, Kay and colleagues were perfectly situated to test this idea. So they collected paste samples from the anal scent pouches of 16 lactating hyenas. (You need a reliable tranquilizer dart gun for this step.)

Back home the samples were analyzed. Bacteria could be seen under high magnification as well as tiny, lipid-containing droplets—the hyena’s gift of food to the bacteria. To identify the bacteria by species, the sample were screened for 16S rRNA genes. This is the DNA that codes for a piece of the ribosome and which is useful in constructing bacterial phylogenies. The genetic survey identified a rich assortment of bacteria from 78 different genera. More than half the bacterial DNA sequences couldn’t be classified—they appear to be new to science. Goes to show what cool new stuff you can find when you get far enough up a hyena’s butt.

And what of the fermentation hypothesis of chemical recognition? All four clans from the Masai reserve had the same types of bacteria; what varied between clans was the proportion of various types of bacteria. Three of the four clans had statistically distinctive bacteria profiles; the fourth did not. By showing that the most prominent bacteria in the scent gland are known producers of short-chain fatty acids—key to odor differences between hyena clans—Kay and colleagues have provided a critical piece of evidence supporting the hypothesis.

The study discussed here is “Evidence for a bacterial mechanism for group-specific social odors among hyenas,” by Kevin R. Theis, Thomas M. Schmidt, & Kay E. Holekamp, published in Scientific Reports 2:61, 201. It can be downloaded here for free.

5 comments:

TheCellularScale said...

So why do the different clans have different proportions of bacteria species?

Avery Gilbert said...

TheCellularScale:

Excellent question. Here's how the authors answer the reverse question: how do clan members come to have similar bacterial communities?

Group-specific microbial communities—and consequently odor profiles—among social animals could be a product of shared environments (e.g. cross-infection), host genetic similarity (e.g. family groups), or, a product of repeated interactions between these two mechanisms. Spotted hyenas frequently scent mark the same grass stalks as their clan-mates (i.e. overmarking), and
they often do so in rapid succession to one another. For hyenas, therefore, overmarking appears to be a viable pathway for the transmission of bacterial communities among members of hyena clans.


[References omitted.]

olfacta said...

My parents had a dog like that once.

Avery Gilbert said...

Olfacta:

Heh.

I scent mark my backyard all the time. Doesn't seem to impress the groundhog.

TheCellularScale said...

Interesting! I wonder how stable these differences are over time. Do the proportions of bacteria and consequently the smell of the clan persist over months, years, or even generations? Hmm I never thought I would be so curious about the hyena's butt.