Male Chauvinist Chimps or the Meat Market of Public Opinion?

Female chimpanzee with her infant requests meat after a successful hunt.

Image: David Bygott / Tree of Life Web Project

Owen Lovejoy's recent paper about Ardipithecus ramidus and human origins (see my detailed critique here) bases its argument on the male provisioning observed in chimpanzees. However, what went unacknowledged in his theory was the inherent gender bias it represented. A perfect example of this was observed in April with the release of the very study on provisioning behavior that Lovejoy used as the basis for his idea.

From the press introductions alone, you would have thought you were in a 19th-century gentleman's club enjoying cigars and brandy. "There's nothing like a prime rib dinner to boost a guy's chances of getting lucky," boasted ScienceNOW as he cleaned his monacle. The Daily Mail agreed with a harrumph, "As every Romeo knows, laying on a delicious dinner for two is one of the best seduction ploys." Chuckling along with a wink and a nudge, MSNBC added, "A savory meat dinner goes a long way, as in all the way."

Ostensibly, these articles were talking about chimpanzees, but it was made perfectly clear what they were getting at. Rupert Murdoch, naturally, got straight to the point. "The oldest profession isn't restricted to humans," FOXNews asserted, while The New York Post headline simply shouted "Chimpanzee Meat Market."

In other words, dating is just another form of prostitution and evolution proves that he that pays gets play. For some reason the barriers were down. Talking about chimpanzee sexuality allowed journalists to let loose and express views they would rarely utter otherwise. Evidently people got the message, if the comments on Slashdot are any indication. A rare case of maturity could be found at The Great Beyond which wrote that:

News that female chimps mate more frequently with male chimps that share their meat with them has prompted a slew of at best corny, at worst downright sexist, even lewd, headlines.

The main problem was that, while everyone else was busy giggling over these chauvinist fantasies, they missed the real meat of the story.

The study in the journal PLoS One, by Cristina Gomes and Christophe Boesch of the Max Planck Institute for Evolutionary Anthropology, finally answered a question that has intrigued primatologists for nearly two decades. Do female chimpanzees preferentially mate with males who share their hunting gains with them? This hypothesis was first suggested in 1994 by Craig Stanford and Jane Goodall when they found that the best predictor for whether males would engage in a hunt or not was the presence of females with sexual swellings (large, fluid-filled sacs indicating the estrous phase of their reproductive cycle). However, subsequent studies could not find any evidence that hunting resulted in direct fitness benefits.

According to a study by Mitani and Watts, females with sexual swellings only received meat on 23 occasions out of 68 attempts and, of those, just 14 resulted in matings. Only a third of all estrous females got meat when they tried for it. In contrast, males were almost four times as likely to share meat with another male involved in the hunt than with an estrous female. When meat was shared with an estrous female, only slightly more than half chose to mate with the male who offered it. The "meat-for-sex" hypothesis appeared to be flaccid. And yet, strangely, there were few sensationalist news reports touting evidence of bromance among our evolutionary cousins.

However, Gomes and Boesch suggested a different approach. What if females remembered the male who shared with them and chose to mate with them at a later time? Over a period of 22 months in the Taï Forest of Côte d'Ivoire the researchers recorded every case of meat sharing (both with estrous and anestrous females), noted who was sharing the meat with whom and identified all of the mating partners during the study period. They also measured grooming, sharing of additional food items and the number of times males assisted females in conflicts with other individuals. Their results indicated that:

[F]emales copulated more frequently with males who shared meat with them at least on one occasion, than with males who never shared meat with them.

The authors were able to eliminate all other variables as significant factors except for male rank, which was independent of meat sharing. The final conclusion was that females were expressing two mutually exclusive choices. The authors spelled it out plainly:

Male rank and sharing meat with females had independent effects on male mating success, indicating that females copulated more with males who shared meat with them and with males of high rank.

The larger story lay not in the fact that females preferred to mate with males who provisioned them, but that they were opportunistically shifting their mating strategies for their own reproductive interests. In earlier studies by Boesch at the same site it was demonstrated that 84% of undesirable advances were rejected by females (Stumpf & Boesch 2006; pdf here), promiscuous mating was reserved for the early part of estrous and that 93% of all copulations were terminated by females (Boesch et al. 2006; pdf here). Females chose who they would mate with, when they would mate with them and how long it would last.

Crucially, as Boesch also determined, ovulation generally occurred between five to eight days after maximum tumescence (when their sexual swellings were largest). By focusing on promiscuous mating in the early part of estrous, females were effectively ensuring that fertilization was less likely. In the later part of estrous females preferred a selective strategy and were much more likely to engage in "consortships" (where a female and male dyad would disappear for several days). This would ensure that the desired male ended up being the father of her child. As a result of these flexible strategies Boesch found that alpha male mating success fluctuated wildly, ranging from 67% to 38% over a 14 year period (Boesch et al. 2006; pdf here). These same shifting and opportunistic strategies have also been observed in populations at Mahale and Gombe.

Unfortunately, this study by Gomes and Boesch didn't measure when in the estrous cycle females chose to mate with males who shared their hunt. It may be that females were reserving the early period of estrous for them and the more fertile period for males of higher rank. However, it could also be that those who demonstrated themselves willing to share were viewed as a better long-term investment. The bottom line however is that females were the ones calling the shots, and males understood that there were only two ways to prove they were serious.

Rather than such hackneyed cliches as "Sex sells, even in the rainforest" (Cosmos) or "The way to a chimp's heart is through her stomach" (both Wired and the Chicago Sun-Times) the real story was that female chimpanzees demonstrate flexible and opportunistic strategies to maximize reproductive success.

Furthermore, because the sharing of meat was primarily with anestrous females, and because there was no relationship between the amount of meat provided and the number of copulations, suggesting that this had any connection to prostitution or buying someone an expensive meal in order to "get lucky" was to completely miss the point. In all likelihood, females were using these exchanges to determine who would be the best potential father for her offspring over the long term. High rank has its advantages, but so does the guy who's willing to share.

In Lovejoy's provisioning theory he seems to make the assumption that females are passive players in the evolutionary dance. In reality, like Ginger Rogers, they are matching every move by Fred Astaire step for step (backwards and in high heels no less). The argument that male provisioning alone would bring fitness benefits, and so much so that it's responsible for the origin of bipedalism, can't even be supported in chimpanzees let alone a species that lived 4.4 million years ago. In many ways it demonstrates the same kind of gender bias that has plagued evolutionary research for the last 150 years.

As Frans de Waal wrote in relation to Lovejoy's theory:

Like the "killer ape" theory, which has been around equally long, the monogamy-bipedality theory focuses entirely on the male (pair-bonding serves to avoid male conflict, which then leads to offspring care, which requires walking on two legs for males to provide food to the family) as if not females, such as Ardi, became bipedal at the same time. What good did it do for them to walk upright? I would very much prefer theories that explain the behavior of both sexes!

Author's Note: This post originally appeared in slightly different form at Nature Network. It was subsequently selected as a PLoS One Pick of the Month and was a Finalist in the 2009 Quark Prize in Science.

Reference:

Gomes, C., & Boesch, C. (2009). Wild Chimpanzees Exchange Meat for Sex on a Long-Term Basis PLoS ONE, 4 (4) DOI: 10.1371/journal.pone.0005116