Eve Davidian: Why do the top dogs get the prettiest ladies? A story of sex, stress and hyena poops

In this new post, Eve Davidian and colleagues explore The interplay between social rank, physiological constraints and investment in courtship in male spotted hyenas. Their study shows that the social and mating system of spotted hyenas may shed some light into the roots of reproductive inequalities in mammalian societies.

Toleo la Kiswahili linapatikana hapa.

In most animal societies, resources are not shared equally among members of a group. Those at the top of the social hierarchy eat the tastiest food, get the comfiest sleeping spots, and can hang out – and more if they hit it off – with the most attractive and fertile mates. In the animal world, where lifetime achievement is largely determined by the number of offspring one leaves behind, it is rather straightforward why individuals should work hard to reach the top and remain there for as long as they can.

Females usually give birth to one or two (rarely three) cubs per litter; when cubs are a few weeks old, mothers translocate them from their isolated ‘birth den’ to the communal den where they socialise with their peers, and occasionally produce these irresistible piles of cubs (Credit: Oliver Höner)

What we still don’t quite understand is how social rank influences reproductive success. Do high-ranking males sire more offspring and offspring of higher quality because they are stronger and more attractive? Or is it because they are less “stressed” by competition with other males and can invest more in courting females?

To answer these questions, we did fieldwork in the African savannah… Lots of fieldwork. Over 20 years – and nearly 20 months of my PhD – searching, identifying, assessing paternities, and monitoring the behaviour of thousands of free-ranging spotted hyenas from the eight study clans in the Ngorongoro Crater in Northern Tanzania. We also collected over 400 steaming hyena scats to measure the concentration of cortisol metabolites, an estimate of the physiological costs – or so-called “stress” – borne by a hyena.

Collecting faecal samples takes a lot of patience and a good eye. But even the highest dedication does not guarantee that you will get a sample; some males like Lampone (centre) are particularly fond of doing it in ponds where their poops are forever lost to science (Credit: Eve Davidian)

We found very clear evidence that interactions with other males are more stressful for low-ranking males than for their high-ranking rivals and that this restricts the time and energy they can invest in courting the most fertile – and most contested – females. We also found that males have to juggle romance and more mundane duties like getting acquainted with new clan mates and maintaining old friendships and strategic alliances. But low-ranking males shy away from these stressful activities and spend more time on their own, munching on bones or chilling in stinky puddles. High-ranking males, on the other hand, need less time on their own to detox and destress, and can invest a lot more in fostering friendly relationships with females. And that’s something hyena females are very much into.

In spotted hyena society, romance is largely dictated by what the females want. In contrast to males of most other mammals male hyenas cannot sexually coerce females because female genitals are masculinized into a rape-proof device. Being friendly turns out to be more effective (Credit: Oliver Höne)

Another very neat result was that philopatric – “stay-home, mama’s boys” – males prioritise reproduction over the fostering of social ties, and focus their reproductive efforts on high-quality females – a likely consequence of their native status and higher social rank compared to immigrants. These results very nicely match our previous work on the fitness consequences of male dispersal strategies where we found that philopatric males reproduce earlier than immigrants and sire offspring almost exclusively with top ranking females.

In contrast to many species where males use their physical strength, long horns and sharp teeth to deter rivals – or even to sexually coerce females – male spotted hyenas do not engage in violent fights to get to the top of the hierarchy and to sire offspring. Why then are low-ranking males more stressed out than high-ranking males?

Displays of dominance can be subtle in spotted hyenas as it often relies on signals rather than aggressive acts. Here, the three hyenas ‘social sniffing’ with their tail up are signalling to the other hyena that they form a tightly knit coalition and should not be messed with (Credit: Oliver Höner)

Male hyenas may not be ruthless brutes but they are no peaceful hippies either. In a recent study, we showed that dominance relationships in hyena society are primarily determined by how many social allies a hyena can count on when in conflict with others. Low-ranking males usually are newcomers and lack strong alliances. They are also more vulnerable to being used as scapegoats by others and this is likely to be a major source of stress. Scapegoating is frequent among hyenas (and other animals) and likely serves as a means to release frustration and cope with stress. In hyenas, it often takes the form of a chain of dominance whereby successive males redirect aggression onto another, lower-ranking male (see video below). And when the lowest-ranking male of such a chain has no scapegoat nearby, rushing tail up at an innocent jackal, a rock, or even our research vehicle seems to do the job.

But don’t feel too sorry for low-ranking males. Their time will come. The social rank of male spotted hyenas is determined by a queuing convention. Most males eventually climb the social ladder and get to enjoy the perks of being the top dog.

It is very interesting to see that even in a society where dominance relationships are formalised by strict social conventions, interactions among males can incur physiological costs that are high enough to trigger behavioural adjustments with (costly) reproductive implications. This study reshapes our understanding of how social rank correlates with ‘stress’ and how male-male competition impacts physiology, sociality and fitness. It also provides new perspectives on the potential physiological mechanism underlying the emergence of alternative reproductive and dispersal strategies.

About the author

Eve Davidian at the research cabin in Ngorongoro Crater in Feb 2022 (Credit: Oliver Höner)

I completed this study as part of my PhD with Oliver Höner and Heribert Hofer at the Freie Universität and the Leibniz Institute for Zoo- and Wildlife in Berlin, Germany. Since then, I’ve been exploring several axes of research in behavioural ecology and evolutionary biology, spanning the roots of social inequalities, kinship dynamics, collective dispersal, as well as sexual conflicts and constraints on female mate choice in mammals. I am currently collaborating with a large consortium of scientists – including Elise Huchard, Martin Surbeck, Dieter Lukas, and Peter Kappeler – on the ecology and evolution of power relationships between males and females in mammalian societies. So stay tuned!

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