Chances are you spent some of your teenage years fretting about your social status. You may have even taken steps to change your status. New haircut. New clothes. These are very human behaviors: our complex social constructs include innate desires to broadcast information about ourselves to our peers.
The nose knows
Science has added layers to these superficial displays, pressing us to consider factors that influence these social broadcasts. It turns out that a significant fraction of these communication signals come from of organic chemicals secreted by scent glands! Now, whether or not humans secrete significant amounts of behavioral scent-based signals is still be a matter of colorful debate. However, for our mammalian kin, the debate is over: the nose knows!
Our true language
Humans aside, mammals are infamous for their use of chemical secretions to convey information. Mammalian scent glands produce a treasure trove of complex organic chemicals for others to detect. That these chemicals have real communicative potential is not controversial. Nevertheless, how these chemical signals vary among individuals and the consequences of this variation are hotly debated. Many theorize that bacteria actually influence the types of chemicals secreted by glands (and the type of message communicated). After all, these glands are warm and sheltered environments for anaerobic microbes, which can ferment organic substrates and spit out communicative byproducts. This creed, known as the fermentation hypothesis, posits that bacteria are responsible for individual variation in glandular secretions.
No laughing matter
Pretty talk, but does the fermentation hypothesis hold water? To examine this we need creatures with potent scent glands and the right social structure to test its assumptions. Which is why, on the eighth day, God made hyenas! These canine relatives sport some pretty potent scent glands, and new field studies indicate that these odorous secretions have a lot to say about bacteria and chemical communication.
These field studies, published late last year in the Proceedings of the National Academy of Sciences of the United States of America (http://www.pnas.org/content/110/49/19832.abstract), investigated the chemical secretions of scent glands beneath hyena tails (termed ‘subcaudal glands’). Their target species were East African Spotted Hyenas (Crocuta crocuta) and Striped Hyenas (Hyaena hyaena). The research team (led by Kevin Theis and Thomas Schmidt at Michigan State University) used the Illumina 454 platform to sequence 16S rRNA genes from bacteria in individual hyena subcaudal glands. These sequences revealed that a vast majority of subcaudal residents are anaerobic fermentative bacteria, just the type of microbes you would expect to ferment substrates into volatile (and communicative) chemical compounds.
As a matter of fat
Both the Spotted and Striped Hyenas use subcaudal secretions to mark plants in their territory, indicating that these compounds have some importance to their social structure. In the study mentioned above, Theis et al. analyzed the volatile fatty acids within subcaudal secretions by gas chromatography and mass spectrometry. They identified multiple differences in the volatile fatty acids between Spotted and Striped Hyenas, which paralleled differences in the 16S bacterial content of these glands.
Among Spotted Hyenas, individuals harbored significantly different varieties of fermentative bacteria and volatile fatty acids in their subcaudal glands. Looking within extended families, Spotted Hyenas of the same sex, or reproductive state, had similar populations of fermentative bacteria and volatile fatty acids in their glands. These findings lend critical support for the fermentation hypothesis. Glands harbor different types of bacteria and scent messages based on the sex and reproductive state of Spotted Hyenas. These glandular bacterial residents may be responsible for the different chemical messages transmitted by their secretions.
The picture is greyer for Striped Hyenas. Their subcaudal gland bacteria and secretions showed less variation by sex or reproductive state. Superficially, these findings might weaken the fermentation hypothesis. But, Striped Hyenas are more solitary, and do not live in large and complex extended family groups like their spotted cousins. Thus, Striped Hyena secretions might simply have less to say.
Smells like bacteria
These observations suggest that the fermentation hypothesis is true. Mammals may use bacteria to influence the secretions of major scent glands. In hyenas, these scents vary by physiology and social status, including sex and reproductive state. But do these differences influence hyena behaviors? The next study will have to investigate this crucial question. This begs even more questions: what factors influence the bacterial content of our glands? Sex hormones? Nutrition? Mutational load? These could be issues to ponder the next time you’re out on a date!