Less aggression when females rule


By Eve Davidian and Oliver Höner

The stronger and more aggressive sex dominates the weaker sex? This simplistic view of male-female dominance relationships is common but falls short of the complexity of how dominance hierarchies are established in animal societies. In our recent study we teamed up with 18 scientists to compare male-female dominance relationships in nine species of mammals, including seven primates, rock hyraxes and… spotted hyenas! The collaborative study revealed that in female-dominated societies, male and female group members relied on submissive signals and gestures to establish and maintain dominance, whereas in male-dominated societies, aggressive behaviours prevailed.

Organising the social life in a group around a clear dominance hierarchy, where each group member knows where they stand, is an effective way to avoid escalated violence and injuries in many animal societies. These hierarchies can be derived from the outcome of agonistic interactions between group members; the individual who shows submission to another will be considered as the subordinate of the pair.

Until recently, most studies of dominance and power focused on ‘intrasexual’ hierarchies, which are derived only from male-male or female-female interactions. This implies that males and females live in separate worlds. They obviously don’t: males and females of many group-living species do compete over the same resources and frequently interact. By studying the sexes separately we are missing out on key aspects of the social and sexual life of animals. Also, because scientists working on different species often used different methods and behaviours to construct animal hierarchies, any attempt to compare patterns between species has been a blurry dream.

In a first step to facilitate comparisons, our colleagues and ourselves compiled field behavioural observations from nine mammal species. We determined the outcomes of 11,499 agonistic interactions among males, among females, and between males and females. We then applied a set of commonly used methods to rank all members of a group relative to one another and construct the ‘intersexual’ dominance hierarchy for each study group and species. Based on these hierarchies, we then calculated the degree of female dominance over males using five different indices.

With our collaborators, we found that the rank order of individuals in the dominance hierarchy was the same irrespective of the methods used and that all indices of female dominance were well correlated with each other. These results are very encouraging because they indicate that the hierarchies and resulting degree of female dominance that are inferred from these methods and indices are robust and comparable. Another very neat result is that our data confirmed that intersexual dominance varies along a continuum from strict male dominance (in chacma baboons) to strict female dominance (in Verreaux’s sifakas) and encompasses species where males and females may share power and ‘co-dominate’. Our results also confirm that the degree of female dominance may vary from one group to the other within the same species. This was particularly prominent in vervet monkeys and rock hyraxes. [discover here our findings showing similar variation in spotted hyenas!]

In a second step, we investigated whether there was a relationship between the degree of female dominance in a species and its ‘dominance style’, that is, whether individuals rely more on certain types of behaviours than others to establish and maintained their dominance relationships. For this, we first had to standardise how we labelled behaviours across the nine species.

Standardisation is key for comparisons. Each species behaves in its own, unique way and because given acts and signals may mean different things in different species – e.g., an individual putting its tail up is considered an aggressive signal for spotted hyenas whereas it is considered a submissive signal in chacma baboons. We therefore divided behaviours into four standardised categories which we then used for the analyses:

  1. Aggressive Acts: e.g., chase, bite, stand over;
  2. Submissive Acts: e.g., retreat, jump aside;
  3. Aggressive signals: e.g., tail up (spotted hyenas), stand up, stare;
  4. Submissive signals: e.g., tail up (chacma baboons), grimace, ears flat, grunt vocalisation.

Our results revealed striking differences in dominance style depending on whether the society was mostly dominated by males or by females. The higher the degree of female dominance in a species, the less frequently animals used aggression to establish and maintain their dominance relationships. More specifically, in strongly female-dominated species, such as spotted hyenas, animals of both sexes more often display submissive signals and less often use aggressive acts compared to male-dominated species, such as chacma baboons, where aggression predominates. So long to the sticky idea that spotted hyenas – in particular the females – are hyper-aggressive beasts…

These results suggest that there are structural differences between male- and female-dominated societies, which very interesting and surely worth investigating in greater detail. With this work, we show that we have robust methodological tools to study intersexual relationships in group-living species in a standardised way. This constitutes a stepping stone towards more conceptual studies such as studies on the ecological and evolutionary causes of variation in intersexual dominance within and across animal societies.

Original publication

Kappeler PM*, Huchard E*, Baniel A, Canteloup C, Charpentier MJE, Cheng L, Davidian E, Duboscq J, Fichtel C, Hemelrijk CK, Höner OP, Koren L, Micheletta J, Prox L, Saccà T, Seex L, Smit N, Surbeck M, van de Waal E, Girard-Buttoz C (2022) Sex and dominance: How to assess and interpret intersexual dominance relationships in mammalian societies. Frontiers in Ecology and Evolution 710.

Further information

Davidian E*, Surbeck M, Lukas D, Kappeler PM, & Huchard E* (2022) The eco-evolutionary landscape of power relationships between males and females. Trends in Ecology & Evolution 37(8):706-718.

Vullioud C*, Davidian E*, Wachter B, Rousset F, Courtiol A*, Höner OP* (2019) Social support drives female dominance in the spotted hyaena. Nature Ecology & Evolution 3:71-76. *contributed equally

Why do the top dogs get the pretty ladies?


A story of sex, stress and hyena poops

By Eve Davidian

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 fecund 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 try to remain there for as long as they can.

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 of searching, identifying, assessing paternities, and monitoring the behaviour of thousands of free-ranging spotted hyenas in the Ngorongoro Crater in Northern Tanzania. We also collected over 400 steaming hyena scats to measure the concentration of cortisol, an estimate of the physiological costs – or so-called “stress” – borne by a hyena. [To know what it takes to be a hyena poop hunter click on the poopers below.]

In our study published in the journal Functional Ecology, we demonstrate 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 fecund – 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 away from other clan members, munching on bones or chilling in stinky puddles. High-ranking males, on the other hand, need less time on their own to detox and de-stress, and can invest a lot more in fostering friendly relationships with females. And that’s something hyena females are very much into!

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 male reproductive skew and 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 [males couldn’t coerce females even if they wanted to because female genitals are masculinized into a rape-proof device]. Why then are low-ranking males more stressed out than high-ranking males?

Male hyenas may not be ruthless brutes but they are no peaceful hippies either. 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. 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.

Our results reveal 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. Our 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.

Original publication:

Davidian E, Wachter B, Heckmann I, Dehnhard M, Hofer H, Höner OP (2020) The interplay between social rank, physiological constraints and investment in courtship in male spotted hyenas. Functional Ecology

Further information

Davidian E, Courtiol A, Wachter B, Hofer H, Höner OP (2016) Why do some males choose to breed at home when most other males disperse? Science Advances 2 e1501236.

Davidian E & Höner OP (2021) A king among queens. Frontiers EcoPics. Frontiers in Ecology and the Environment 19(10): 573.

Höner OP, Wachter B, East ML, Streich WJ, Wilhelm K, Burke T, Hofer H (2007) Female mate-choice drives the evolution of male-biased dispersal in a social mammal. Nature 448: 798-801.

Davidian E*, Benhaiem S*, Courtiol A, Hofer H, Höner OP, Dehnhard M (2015) Determining hormone metabolite concentrations when enzyme immunoassay accuracy varies over time. Methods in Ecology and Evolution 6(5):576-583. *contributed equally

Friends over muscles: How female hyenas came to dominate males


By Oliver Höner and Eve Davidian

In most animal societies, members of one sex dominate those of the other. Is this, as widely believed, an inevitable consequence of a disparity in strength and ferocity between males and females? Not necessarily. Our new study shows that in spotted hyenas, females dominate males because they can rely on greater social support, not because they are stronger or more competitive in any other individual attribute. The main reason for females having, on average, more social support than males is that males are more likely to disperse and that dispersal disrupts social bonds. This study was conducted in collaboration with the Institut des Sciences de l’Evolution de Montpellier (ISEM-CNRS, France). Our results were published in the journal Nature Ecology & Evolution.

Spotted hyena females are often portrayed as archetypes of powerful and ferocious females. They are on average heavier than the males, have highly masculinised outer genitalia (a ‘pseudo-penis’ and a ‘pseudo-scrotum’), and usually occupy the highest position in the society. But according to the new study, it is not their manliness that allows them to dominate males.

When two hyenas squabble, the one that can rely on greater social support wins, irrespective of sex, body mass or aggressiveness. Differences in social support between two individuals correctly predicted who will be the dominant in almost all encounters and in all contexts – between natives and immigrants, members of the same and different clans, residents and intruders, and individuals of the same and opposite sex.

Female dominance thus emerges from females being more likely to receive greater social support than males. What is so fascinating is that it all works without any direct involvement of other hyenas. In the end, it’s all about assertiveness and how confident a hyena is of receiving support if needed.

08_07a_Blog_Female dominance_crop

For this study, our team analysed the outcome of 4133 agonistic interactions between 748 hyenas from eight different clans monitored for 21 years in the Ngorongoro Crater in Tanzania. To estimate potential social support, we developed an algorithm that predicted for each clan member, which of two interacting hyenas it would support; this algorithm was derived from behavioural observations of social support and relatedness estimates based on one of the most comprehensive pedigrees of a free-ranging mammal. To tease apart the effects of social support and intrinsic attributes such as body mass, one needs to evaluate each effect while controlling for the presence of the other. When this is done, the effects of sex and body mass appear negligible.

Clear dominance relationship

In many social contexts, female and male hyenas can rely on equal social support and are equally likely to win. But there is one exception: when natives interact with immigrant clan members. Hyena society is highly nepotistic and social support is primarily given to kin. Native clan members live among their relatives and have a competitive advantage over immigrants because immigrants lose their social bonds when they disperse from home. In this context, females have the upper hand because immigrants are usually males.

Female dominance in spotted hyenas is therefore driven by the sex bias in dispersal and the demographic structure of the clan: when the clan contains a high proportion of immigrant males, female dominance is nearly absolute. But when the clan contains many native males, males win almost as often as females and the sexes are co-dominant.

Implications of the study:

Identifying the determinants of dominance relationships between the sexes is fundamental to understanding the evolution of reproductive strategies, gender roles, and sexual conflicts. Our findings show that social dominance of one sex over the other – a trait that characterises gender roles – does not need to be a direct consequence of sex or physical strength, but can be shaped by the social environment.

By demonstrating the key role of social support in mediating the establishment of dominance – and sex-biased dominance – the study improves our understanding of the social impact of nepotism, political alliances, as well as emigration and immigration patterns in animal and human societies.

Original publication

Vullioud C*, Davidian E*, Wachter B, Rousset F, Courtiol A*, Höner OP* (2019) Social support drives female dominance in the spotted hyaena. Nature Ecology & Evolution 3:71-76. *contributed equally

Media outlets

Hyena girl power explained. CNRS-news, 19th November 2018.

Further information

Davidian E, Courtiol A, Wachter B, Hofer H, Höner OP (2016) Why do some males choose to breed at home when most other males disperse? Science Advances 2 e1501236.

Höner OP, Wachter B, East ML, Streich WJ, Wilhelm K, Burke T, Hofer H (2007) Female mate-choice drives the evolution of male-biased dispersal in a social mammal. Nature 448:798-801.