Hyenas’ social status shines through in their poop

Everybody poops, as the saying goes. So it’s easy to think of poop as a class unifier that brings animals together across divides. Scientifically speaking though, it’s not–at least when it comes to hyenas. Spotted hyenas of high and low social status have acquired epigenetic differences, detectable in their scat, according to new research. In other words: Biologists can discriminate between high and low ranking hyenas through feces analysis, finding “molecular signatures of social status,” per a study published March 28 in the journal Communications Biology.

In hyena society, some individuals dominate over others. The resulting ranks determine how animals interact and acquire food. Higher status hyenas can be seen as more popular, engaging in more frequent and successful social contact. They also have to put in less work to eat. The new study shows these social norms have far-reaching effects, even altering how an animal’s DNA is expressed.

When the environment affects genes

These DNA alterations come in the form of epigenetic changes, or shifts in how genes are expressed in response to environmental conditions. At 149 epigenetic sites within gut cells extracted from scat samples, high status and low status hyenas show significant differences.  Between the two groups of animals, consistent variations in DNA methylation–a process where methyl groups bind to regions of the genome within a cell, and silence certain genes–are detectable.

Lots of things influence DNA methylation–much of it is inherited, but some of it is acquired throughout life. Things like food availability, activity level, stress, competition, or exposure to pollutants can all prompt changes in methylation, and thus gene expression. Once epigenetic changes have occurred, some can be passed down to the next generation.

In hyenas and a few other species of animals, prior research has hinted that social status can lead to epigenetic shifts. The new study builds on that previous work, confirming the phenomenon in a clan of wild hyenas with novel methods, identifying the genes modulated by methylation, and showing changes in both cubs and adults. The study adds to the growing body of evidence that the social environment plays a significant role in animal and human health and physiology, leaving a long-term mark on DNA.

It’s a “well done study” that improves on past work with more sensitive techniques, says Christopher Faulk, an associate professor of genetics at University of Minnesota who was uninvolved in the new research. Faulk previously contributed to research on DNA methylation in spotted hyenas, but he says that, thanks to advances in genetic science and the clever idea of turning to scat instead of blood or organ tissue, the new study represents “an impressive technical feat.”

“If we were to re-do our study today, we would have done it exactly this way. I think it [uses] excellent methods,” he adds.

Molecular traces of social order

Hyenas live in female-dominated clans organized under a strict social hierarchy. Higher-status individuals subordinate lower-status ones, and rank is passed down from mother to daughter. The social order determines things like how conflicts are resolved and also how far an individual has to travel to forage–higher status animals have priority to closer food sources, while low-status hyenas have to commute longer distances.

It’s these differences in resource access that the scientists hypothesize are triggering epigenetic changes, even for young cubs. Low-status mothers traveling for food spend less time nursing their offspring than mothers that get to stay closer to the den, explains senior study author Alexandra Weyrich, head of wildlife epigenetics at the Leibniz Institute for Zoo and Wildlife Research in Berlin, Germany. “It’s a very early imprint” of social status, she says.

Weyrich and her co-author’s findings support that idea. The biologists collected and analyzed fresh scat samples from 42 different hyenas, 18 high-ranking females and 24 low-ranking females–both cubs and adults. They extracted DNA from gut epithelial cells in the poop piles and identified 149 regions of differential methylation between the high and low status groups. Much of epigenetic work relies on more invasive methods, like drawing blood or taking tissue samples. By using feces, the researchers were able to avoid stressing or endangering the study subjects. “We didn’t have to interfere with the animals,” Weyrich says. “This [method] has never been done before [in the wild]…it opens up a big way forward for other researchers that work on wild species as well.”

Many of the genes the researchers homed in on through their analyses are related to energy conversion, the immune system, and gut-brain communication–signaling that the food access and other status differences have long-term effects on hyena metabolism and health. They further found methylation differences in both cubs and adults, with new epigenetic changes emerging in maturity. In a complementary series of tests performed on samples from the same clan, the study authors were able to identify whether a hyena was high- or low-ranking from methylation signatures alone with 80% accuracy. Though compelling, the study relies on a small sample size of associated hyenas. “It’s a nice result,” says Weyrich, “but it needs to be tested on other populations” to prove the pattern, she adds.

From hyenas to humans

“Wild hyenas actually serve as a fantastic model for humans,” says Faulk, because of their nuanced social dynamics and behavioral complexity. He conducts lots of epigenetic studies in laboratory mice, but says hyenas offer a different level of insight. “They’re not under the artificial manipulation of either a laboratory or domestication.”

Lots of research in humans and rodent studies indicates that early life experiences can lead to epigenetic shifts. Though it’s not a direct one-to-one comparison, the new study “can be extrapolated” to people, says Weyrich. “We have to be a bit cautious,” she adds–noting that more research would be needed and that the exact gene regions under epigenetic pressure may differ, but the study does suggest social rank and resource access have significant bearing on mammal gene expression. Despite the specifics of different species’ social hierarchies, if it’s happening in hyenas, it could be happening in humans too.

“This hyena research directly contributes to our understanding of how the human social environment might impact our health and risk of disease,” says Faulk. “It’s a very useful and important line of study.”

Update 03/28/2024 1:29PM: Some terminology has been adjusted to clarify the difference between epigenetic and genetic change and more accurately describe hyena social structure.