The story begins with an insurrection, and ends with infanticide. A male gelada monkey, unsatisfied with his social standing, challenges the authority of a superior gelada. The payoff: a so-called "reproductive unit," comprising a dozen females, that will mate with him and him alone. If the usurper is victorious, he will kill any offspring that were sired by his predecessor.
It's a fierce and violent overthrow, to be sure, and it's a social dynamic that scientists have been investigating for decades. But now, researchers studying a population of wild geladas in Ethiopia have discovered an element of sacrifice in this story of subversion and murder. It turns out that female geladas will actually terminate their pregnancies when a new male takes charge of their unit. But in the process, these monkeys actually increase their evolutionary fitness.
The Bruce Effect
This is not the first time researchers have observed this curious biological mechanism. Over fifty years ago, biologist Hilda Bruce published the first evidence of what would later come to be known as the "Bruce effect" — a phenomenon whereby a pregnant female will terminate her pregnancy when exposed to a new male.
Bruce first recorded the event in mice, and while her results have since been replicated in a handful of other taxa, every one of these investigations has been performed under carefully controlled lab conditions. To date, not a single experimental study has provided conclusive evidence of male-induced pregnancy termination in a non-captive setting, leading many to conclude that the Bruce effect is little more than an aberration brought on by a laboratory setting. But now, it looks as though the skeptics may have their proof.
In the interest of addressing the dearth of evidence for the Bruce effect in wild populations, a research team led by University of Michigan's Jacinta Beehner spent more than five years surveilling geladas in Ethiopia's Simien Mountains National Park. The group followed a total of 110 females from 21 different reproductive units, and witnessed the overthrow of 28 gelada males.
When the researchers examined birth patterns within groups that had undergone male takeovers, an incredible pattern emerged. In the six months leading up to a takeover, birth rates were identical to those in groups that had not experienced a male replacement within the previous year (the gestation period in geladas is a little over six months, so any offspring born to these control females would not have been susceptible to infanticide).
But in the six months following an exchange in power, birth rates plummeted.
The researchers observed just two instances where infants sired by a predecessor were born following a new male's arrival, compared to thirty-six in control groups. Hormone sampling confirmed that this devastating drop in birth rate was due to pregnancy termination. By measuring hormone levels in the feces of female geladas, the researchers were able to track a total of 60 pregnancies, of which nine ended in failure. Eight of these terminations occurred in the 2 weeks following a male replacement — and Beehner says it's likely there were even more terminations that simply couldn't be accounted for.
"Our non-invasive pregnancy method is a little bit flawed," she explained. "We can't detect pregnancies until around the fourth week of pregnancy. Studies on rodents show that the Bruce effect is most common during the equivalent of the first trimester, so there's probably a much higher rate of first trimester losses that we just can't detect."
While the majority of the terminations took place during the second trimester, they actually occurred during all three stages of pregnancy. The third trimester termination, explained Beehner, "was the most surprising of all. For her to miscarry so late in gestation was totally unexpected."
The cold, hard facts of reproductive fitness
The researchers' surprise at such a late-stage termination gets to the heart of one of the biggest questions to emerge from their findings: why do females miscarry when a new male arrives?
Before we go any further, it bears mentioning that there is no evidence these miscarriages are being performed consciously by the pregnant females; they're simply hard-wired to happen. But for such an adaptation to survive within a population, it stands to reason that terminating a pregnancy in the event of a male takeover must offer some form of evolutionary benefit to the female.
With this in mind, the researchers hypothesize that the Bruce effect has likely evolved as a loss-cutting strategy for pregnant geladas at risk of losing their offspring at the hands of a usurping male. They observed, for example, that females who terminated after a new male took over were able to return quickly to a fertile state, mate with the new male, and bring offspring to term faster than those who didn't, suffering only a minor reproductive delay in the process.
"Even once you're in the third trimester," Beehner explains, "it just doesn't pay to keep investing."
According to ethologist Neville Pillay — who has studied the Bruce effect in captive rats, but was not involved in the study — the argument presented by Beehner and her colleagues is sound. From a cost/benefit standpoint, he explains "termination is better than carrying [the fetus] to term [if it will] eventually be killed by the new male." Even though the female gelada would suffer an immediate loss, explains Pillay, on a long enough timeline, the termination is actually advantageous to her ability to successfully give birth to offspring that will survive.
That being said, such an evolutionary adaptation would only make sense for females in species where male infanticide is a significant risk. By that reasoning, explains Beehner, a Bruce effect almost certainly does not exist in humans; although the mechanisms behind pregnancy termination in geladas (be they regulated by pheromones or by hormonal shifts brought on by stress), could very well hold the clues to understanding pregnancy success across a variety of species — humans included.
In the realm of biology, it is an organism's ability to pass its genetic information on to subsequent generations that is the ultimate gauge of what evolutionary biologists call reproductive fitness. Geladas are no different. This evolutionary principle can explain both the infanticidal habits of usurping gelada males, and the tendency for females to terminate their pregnancies following a successful coup. Female geladas know a thing or two about sacrifice — but their bodies understand the cold hard facts of evolutionary success.
The researchers' findings are published in today's issue of Science.
Top photo and reproductive unit photographed by Clay Wilson; mother gelada and offspring photographed by Shayna Liberman; all photos via AAAS/Science