BEACON Researchers at Work: Coevolution of hyenas and their beneficial, odor-producing bacteria

This week’s BEACON Researchers at Work post is by MSU postdoc Kevin Theis.

Kevin Theis with an anesthetized adult male hyena named Detroit.

My research, conducted in collaboration with Michigan State University and BEACON researchers Kay Holekamp, Tom Schmidt and Tracy Teal, lies at the intersection of two broad ideas that have BEACON’s mission of studying “evolution in action” at their core.

The first idea is that many, perhaps even all, animals can be appropriately viewed as supraorganisms. A supraorganism is an organism that is actually a composite of multiple contributing organisms. Consider yourself, for example. There are roughly 100 trillion cells and 3 million genes associated with your body. Amazingly, ninety percent of those cells and ninety-nine percent of those genes are bacterial. You are simultaneously a veritable ecosystem, affording a stable home to multiple generations of trillions of bacteria, and a supraorganism because those bacteria are having as great an effect on your biology as you are having on theirs! Obviously, some of these bacteria are detrimental to your health, but most are truly beneficial. For example, your symbiotic bacteria were instrumental in the proper development of some of your tissues, they primed your immune system against many pathogenic bacteria, and today they continue to competitively exclude additional pathogens and to provide you with critical vitamins and nutrients. Furthermore, recent research suggests that your microbes can affect your behavior in beneficial ways as well, a phenomenon that likely pertains to most members of the animal kingdom.

The second idea is that communication is the glue that holds animal societies together. Many animals are social because, at a functional level, they reap fitness benefits from living in prolonged and close proximity to conspecifics. Specifically, they benefit from decreased predation risk, increased foraging efficiency, greater access to potential mates, and improved ability to secure and defend limited resources. However, there are also costs inherent with living in societies, most notably increased competition over “shared” resources. The adhesive quality of communication stems from its value in facilitating the benefits and modulating the costs associated with living in animal societies. Again, you yourself provide an excellent example, although this time I’ll allow you to walk through the argument on your own.

So, animals can often be appropriately viewed as supraorganisms and communication is the glue that holds societies together, but where do these two seemingly disparate ideas intersect? In a hypothesis suggesting that the bacteria associated with the bodies of many animals underlie the chemical communication systems of those animals, and thus are critical linchpins in the operation and maintenance of those animals’ societies. At a mechanistic level, the idea specifically suggests that the odorants many animals use to communicate with one another are by-products of their symbionts’ metabolisms, and that variation in the information content of animal chemical signals is a direct consequence of underlying variation in the diversity of their bacterial communities.

A spotted hyena pasting a grass stalk in the Masai Mara National Reserve, Kenya.

I am currently studying this idea in the spotted hyena. Spotted hyenas are large carnivores found throughout sub-Saharan Africa. They live in complex societies, called clans, that typically contain 40 to 80 hyenas. Hyena societies are extremely competitive, but unlike most mammalian societies, they are female-dominated and dominance status within clans is not determined by body size or fighting ability. Instead, offspring inherit their mothers’ social ranks. Adult immigrant males, all of whom are subordinate to all natal individuals, must queue for social status. To mediate the complex social interactions both within and among clans, hyenas use a rich repertoire of visual, vocal and chemical signaling behaviors. A common and conspicuous chemical signaling behavior of hyenas is pasting, wherein a hyena straddles a grass stalk and drags its extruded anal scent pouch across the stalk, leaving behind a thin layer of smelly secretion, called paste. At a functional level, pasting helps maintain  clan territories, and also appears to effectively advertise the dominance status of males and the reproductive condition of females.

A scanning electron micrograph of bacteria associated with spotted hyena paste.

To demonstrate that variation in the bacterial communities within hyena scent pouches underlies chemical signaling among hyenas, I am confirming, using next-generation sequencing technologies and gas chromatography – mass spectrometry, that bacterial and odorant profiles of paste co-vary, and that pure cultures of bacteria isolated from the paste of wild hyenas yield the expected odorants. MSU research assistants Kwi Kim and John Dover, and undergraduate students Jacquelyn Dycus and Emily Schmitt-Matzen have been instrumental in this process.

Although, to date, my research has largely explored the ecological aspects of spotted hyenas’ relationships with their bacterial symbionts, coevolution among hyenas and their scent pouch bacteria has always been implicit in the model. Recently, along with collaborators Holekamp, Schmidt and Teal, I have begun to explore the evolutionary aspects of these relationships as well. Specifically, we are using recent advances in bioinformatics to test whether spotted and striped hyenas have coevolved with the bacteria inhabiting their scent pouches. Striped hyenas are largely solitary animals found in northern Africa and the Middle East, although the ranges of the two species do overlap in parts of Kenya, East Africa. Given that the lineages of these two hyena species diverged more than 4 million years ago, the bacterial communities inhabiting their scent pouches should differ. Also, as there is variation in the selection pressures shaping symbiotic communities among body sites, the bacterial communities in the anal scent pouch of a given hyena species should differ from those associated with its other body sites (e.g. nose, mouth, rectum). We have now begun evaluating both these predictions.

Although this evolutionary aspect of my research is in its infancy, it is a direct testament to the strength of BEACON’s mission to bring ecological, evolutionary and computational biologists together to study “evolution in action.”

For more information about Kevin’s work, please contact him at theiskev at msu dot edu.

About Danielle Whittaker

Danielle J. Whittaker, Ph.D. Managing Director of BEACON
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