ABOVE: A male bonobo interacts with a female. Martin Surbeck

Humans tend to assume that across species it’s males that are most able to shape the behavior of others—that is, to wield power.  

But a review published today (May 18) in Trends in Ecology & Evolution suggests that in many species, that’s not the case. The authors propose a new framework for evaluating power distributions between the sexes that takes into account the ways in which they say females often wield power. 

Although males are typically the dominant sex in mammals, the authors note that females obtain power differently than their male counterparts, and that this power depends on the type of mating system the species employs. For example, males in polygynous systems (in which male animals have more than one female mate) are typically in power because they are larger than the females and can use physical force to control them.  

On the other hand, females in polygynandrous systems (where both females and males mate with multiple partners) are favored to hold the power—typically through reproductive control like trading sex for food and prime sleeping spots. An example of this trade can be seen in spotted female hyenas, whose genital structure makes it impossible for males to forcibly mate with them. 

For more on power relationships among mammals, The Scientist spoke with review coauthor Eve Davidian of the Ngorongoro Hyena Project

The Scientist: Can you explain what you mean by power relationships between the sexes?

Eve Davidian: Power can be broadly described as the ability of one individual to influence the behavior of others. When it comes to a relationship between the sexes, you can translate it into the ability of one sex to exert control over members of the other sex. And the type of power that we focused on for this work is what we call resource holding power—that is, the extent of control that one sex can exert over the other over the access to resources like food, or water, or shelter, or even territory. The other type of resource is access to reproduction. And reproductive control is what we would define as the ability to control when you will mate with an individual, who you will mate with, and how many times. 

TS: How does reproductive control promote social control?

ED: The idea is that in many species, at least in mammal species, males are often larger than the females—they are better equipped in terms of weaponry, so they have longer horns or sharper teeth. . . . In terms of male-male competition, the males that are larger or better armed will be able to fight against the other males and usually win. This will allow them, among other males, to win access to females. . . . When females gain some reproductive control, they will be able to escape from males or [use] various strategies that will allow them to counteract these males’ coercive attempts. And they will be able to use this ability that they have to choose who they mate with, to then maybe have some types of exchange because then males will try to do what the female wants [in order] to get what they want. 

See “The Hidden Side of Sex” 

TS: Why did you decide to take a closer look at the power relationships between male and female animals?

ED: First is that historically, power is everywhere—all societies, animal societies, even in our human societies—they are structured by power, and mainly power asymmetries between individuals. Our social dominance, for example, has mainly been studied among each sex, but separately. . . . So we got to know quite well, separately, what was driving the dominance and power relationships within each sex. How males and females interact will determine how the reproductive interactions, the mating system, the social system, the survival of individuals, influence a lot of aspects of animal societies. We wanted to understand what causes and what are the consequences of these relationships, and we had very few tools to try to study that. . . . So we thought that it was quite time to try to synthesize all this work and try to come up with a theoretical framework to try to get some tools to actually study that. 

TS: What are some misconceptions people have about power asymmetries between male and female animals, and why do you think that is?

ED: One of the misconceptions was that for a long time, species were considered either as male-dominated or as female-dominated, so there was this binary vision of power relationships. It’s possible that some of these ideas were partly shaped by the societies in which we live. We know that the questions that scientists ask, the way we address the questions, and sometimes the way we interpret what we observe, can be shaped by the society where we live in and the times where we live. . . . But there is also the fact that . . . most mammals are male-dominated, or at least have been described as such. So it’s possible also that somehow scientists didn't quite see the relevance of digging deeper, because what they observed in mammals kind of confirmed their prior conception that they had that, ‘OK. It’s just male dominated, and that’s the way it is,’ and the few female-dominated species are just anecdotes.  

TS: Why do we see different sexes having more power in different species?

About a dozen hyenas cluster together on the savannah
A group of hyenas
Oliver Höner

ED: What we propose in this study is that it’s largely shaped by which sex has the highest degree of control over reproduction. And this—whether it’s going to be more males or more females [having power]—can be predicted by features of the mating system of the species. We argue that some mating systems favor male ability to coerce and control females, while others are associated with greater female power. For example, on the male-dominated side of the power continuum, you have polygynous systems. That’s where one male reproduces with several females, whereas females usually reproduce just with one male. In this system, males are typically larger than the females, and as described before, they can use their force to exert high control over females. In contrast, in promiscuous systems, like in bonobos or spotted hyenas, males and females can mate with multiple partners during the breeding season, and female power over males is favored. In these systems, females have the possibility to mate with their preferred mates and use their leverage to gain social power. Interestingly, monogamous systems, which we find in meerkats, for example, seem to be egalitarian in that power is shared equally between the sexes. 

See “Opinion: Monogamy and Cooperation Are Connected Through Multiple Links” 

TS: For this review, why were certain animal species [like spotted hyenas and bonobos] looked at specifically?

ED: We tried to do a literature search that would be as comprehensive as possible . . . but the different coauthors are actually empiricists working on specific species like me—I’m working on spotted hyenas, and other authors on lemurs, another one on bonobos, and the other one on baboons. So each of us had special expertise, and each of these species all really [fit] well, because all of them can have a different mating system, a different social system, and different power relationships between males and females. What we realized is that each of these species could be positioned on a continuum of power relationships. 

TS: What can these power relationships tell us about evolution?

ED: Once power is established either as strongly male-biased or strongly female-biased, it seems the power structures are very stable in the evolutionary context. This is because there are positive feedbacks that will reinforce biases in reproductive and social control between the sexes. But sometimes you might have a little change in reproductive control that will destabilize these feedbacks and trigger an evolutionary shift. Species will shift from a male-dominated system to a female-dominated system, or vice versa. And that’s maybe the key to explain why bonobos differ from their—and our—closest relatives, chimpanzees. Chimpanzees live in strongly male-dominated societies, where males have both high reproductive and social control over females. Female chimps have these sexual swellings that signal the onset of their estrous, and it’s very accurate. So males can really focus all their effort on specific females that they know are ready to conceive to make sure that these females will only reproduce with them. This gives them very high social and reproductive power. In bonobos, which are very similar in many aspects to chimps, females also have these swellings, but they are really not accurate because females have these swelling over long periods of time. So female bonobos in fact use these swellings to deceive males. As a result, males don’t really know when it’s a good time to guard a female and to reproduce with the female. This in turn gives females high reproductive control and leverage, which they can use to gain social power. So what seems like a subtle change in reproductive control, with a switch from accurate to deceptive sexual swellings, can have big social consequences.  

TS: What . . . was the most interesting finding or phenomenon you came across while writing the review?

ED: What I thought was quite neat is that this framework that we propose describes power along these two axes of social control and reproductive control. Using this dimensional description of power is quite nice because it’s very new, and especially this causal relationship between reproductive control and social control. This is a very interesting and exciting idea. For me, the other point is more a technical aspect. It’s that really, we built this framework like some sort of toolkit to try to describe and quantify and predict the power relationships between the sexes. . . . So [I’m] quite excited to see how it’s going to be applied to other species and also to test our hypothesis.