I’ll have what she’s having: Manipulation in chimpanzee copulation calls

When we think about animal relationships, some endearing examples of devoted couples come to mind: emperor penguins that faithfully guard their hatchlings for weeks while they wait for their mate to return; love birds (not surprisingly) that groom and feed each other during courtship, and some species of monkeys that intertwine their tails as they sit next to their mates.

However, these types of attentive, faithful relationships are relatively rare in the animal kingdom, as only 5% of mammals are estimated to be monogamous [1]. In fact, even the emperor penguin example that we all know and love has more to the story: although mates are generally faithful to each other within a season, only 15-22% relationships continue through the following year [2].

Rather, many species have mating systems where individuals mate with multiple partners, and deception and coercion are often tools of the trade. These mating systems are important for biologists to understand, as they are often indicative of other factors about a population like resource distribution and parental care, and can demonstrate conflicting reproductive interests between males and females. For example, the female Grevy’s zebras in the dry landscape of northern Kenya must venture to water sources after giving birth, where males that defend these territories are lying in wait to mate with the incoming parched females [3]. While the females’ priorities are to quench their thirst and replenish their energy after a taxing birth, the males attempt to take advantage of this vulnerability and acquire a mating.

The mating etiquette in our closest primate relatives is no better– chimpanzee relationships are also full of coercion, deception, and intrigue.

Chimpanzee males are on the alert for any action their competitors may be getting. Photo credit to Clément Bardot (Wikimedia commons).

Chimpanzees have a promiscuous mating system in which females can mate with most of the males in their community during a single estrous period. In some ways, this works to the advantage of females, because mating with multiple males obscures paternity and reduces infanticide. In other words, when a female gives birth after mating with multiple males, no single male knows whether or not that infant is his, discouraging him from killing it.

On the other hand, promiscuous mating in chimpanzees leads to aggression and coercion from males towards all females, especially the older, more experienced females that are more desirable [4, 5]. Females prefer dominant males, but males of lesser status can still coerce them into mating. This coercion often harms females– in addition to being physically stressful, it is energetically costly to resist a lower quality mate in favor of mating with a more favorable male. Coerced matings also take up time that a female could otherwise be using to engage in other activities like feeding, resting, or socializing. While there is evidence that some females will strategically initiate matings with high-ranking males as a counter tactic to coercion [6], therefore indirectly competing with other females, female chimpanzees are still generally regarded as the passive sex.

So what’s a female chimp to do when all the agency seemingly belongs to the males? This is exactly what researchers were interested in in their 2016 paper in Animal Behavior [7]. While there is little direct competition between females, lead author Brittany Fallon hypothesized that females would use “copulation calls” to reflect their attractiveness in order to indirectly compete with other females for matings with desirable males. These copulation calls are distinct, rhythmic screams elicited by females during or after matings. Previous research in baboons [8] suggested that females use copulation calls to encourage follow-up matings with high-ranking males, and to reduce infanticide risk.

Fallon and her colleagues predicted that less experienced, less attractive females would change their calling behavior depending on the other chimpanzees present. The researchers observed the mating activity of 20 females over nearly 2,700 hours and recorded presence/absence of copulation call, partner identity and rank, audience, and duration of copulation.

They found that overall, less experienced and thus less attractive females were more likely to call than experienced females, particularly during long copulations. While the presence of other females did not affect call length or likelihood, less experienced females became less likely to call as the number of high-ranking males in the audience increased, while experienced females became more likely to call in this situation.

Older females, like this one, are more desirable to male chimpanzees. Photo credit to Derek Keats (Wikimedia commons).

The fact that less-attractive females generally call more than attractive females has a couple of possible explanations. First, while attractive females have less of a need to advertise, less-attractive females have more at stake in a breeding season. Thus, they may call more to encourage high-quality males to mate with them. In contrast, more experienced females may be able to utilize copulation calling more strategically, limiting their calls when the risk of male aggression is high. Furthermore, the fact that inexperienced females called less when the number of high-ranking males increased could be due to their heightened fear of male aggression in response.

Fallon points out that in general the inexperienced females “were not reserved about the fact that they are less attractive sexual partners. These females were constantly seeking males out, and their copulation calls reflect that.” Additionally she notes that “the aggressive calling strategy does not necessarily imply that females consciously assess their attractiveness – they could simply be responding to male interest, or lack thereof.”

These results are interesting because they indicate a flexible strategy for females as a way to exert mate choice even in a system with high rates of male coercion. This means that females, in particular lower-quality females with more to gain, may have more control over their own reproduction than previously thought. While this may not necessarily be a conscious strategy, these results may change the way we think of females in coercive mating systems– less as passive partners, and more so as individuals with tools at their disposal to maximize their reproductive interests.

[1] D. G. Kleiman. “Monogamy in mammals.” Q. Rev. Biol., vol. 52, pp. 39–69, 1977.

[2] J. Bried, F. Jiguet, and P. Jouventin. “Why Do Aptenodytes Penguins Have High Divorce Rates?” Auk, vol. 116, pp. 504-512, 1999.

[3] D. I. Rubenstein. “Ecology and sociality in horses and zebras.” In: Ecological Aspects of Social Evolution (eds D. I. Rubenstein and R. W. Wrangham). Princeton, NJ: Princeton University Press, pp. 282-302, 1986

[4] M. N. Muller, M. Emery Thompson, and R. W. Wrangham. “Male chimpanzees prefer mating with old females.” Curr. Biol., vol. 16, pp. 2234-8, 2006.

[5] M. N. Muller, S. M. Kahlenberg, M. Emery Thompson, and R. W. Wrangham. “Male coercion and the costs of promiscuous mating for female chimpanzees.” Proc. R. Soc. Lond. [Biol.], vol. 274, pp.1009-1014, 2007.

[6] K. Pieta. “Female mate preferences among Pan troglodytes schweinfurthii of Kanyawara, Kibale National Park, Uganda.” Int. J. Primatol., vol. 29, pp.845-864, 2008.

[7] B. L. Fallon, C. Neumann, R. W. Byrne, and K. Zuberbühler. “Female chimpanzees adjust copulation calls according to reproductive status and level of female competition.” Anim. Behav., vol. 113, pp. 87-92, 2016.

[8] S. M. O’Connell and G. Cowlishaw. “Infanticide avoidance, sperm competition and mate choice: the function of copulation calls in female baboons. Anim. Behav., vol. 48, 687-694, 1994.


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