On Prairie Dogs

Not exactly my model species, but I talked about birds a short while ago, so why not prairie dogs? They're at least mammals with strong social organization. Anyway, I paper came to my attention, about dispersal in prairie dogs, and it was published in Science, so of course I had to read it.

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Prairie dogs disperse when all close kin have disappeared

Prairie dogs pull up stakes and look for a new place to live when all their close kin have disappeared from their home territory--a striking pattern of dispersal that has not been observed for any other species.

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Original article is here (behind Science's paywall). As previously discussed, baboons disperse when they are on cusp of full adulthood. They find a new troop, and usually stay with that troop until they die.

Prairie dogs differ from baboons in several striking ways. They live in large groups, called colonies, and the size of these groups can vary quite a bit, which is nothing unusual to a primatologist. But unlike baboons, prairie dop groups can range from five to thousands. Colonies can be further subdivided, into wards, and then coteries. Needless to say, prairie dogs almost certainly do not possess baboons' rich understand of who's who in the group. Nevertheless, these subdivisions are oddly reminiscent of the four-level hierarchy found in Hamadryas baboons.

Coteries are the closest thing there is a basic unit of prairie dogs. Coteries are sort of like harems: they consist of a male, several females, plus juveniles and infants. The juvenile males disperse soon after they are a year old. They leave their natal territory, settling about 1.5 miles away, on average. Females tend to stay put.

The author of this paper, Hoogland, references the esteemed Hamilton and May. Their theory was that dispersal occurs because reducing the amount of competition (for mates, food, etc) between related individuals is good for inclusive fitness. On the other hand, the potential for cooperation between related individuals might outweigh the costs of competition. Over the past few decades, Hamilton and May have been supported by findings in the field.

Hoogland has found contradictory evidence in his prairie dogs. When zero relatives are around, females are much more likely to disperse, 2.5 to 12.5 times more likely.

These prairie dogs have no opportunities for competition between relatives, but also no opportunities for familial cooperation. You might think that the dangers of dispersal would still be a major impediment, but apparently these populations live pretty close together, and the females usually just move one colony over, so the risks are low.

Hoogland's own words, to sum it all up:

"The absence of close kin in the natal territory is thus a proximate cause of natal dispersal by prairie dogs, but the ultimate cause is presumably the opportunity to find either a new territory that offers the benefits of cooperation with close kin that dispersed there previously (rare), or a new territory in which survivorship and reproductive success might be less dependent on cooperation with close kin (common)."

This may not be a study about primates, but the laws of dispersal and inclusive fitness govern all animals. When we discover a behavior violates our conceptions about how life must act in order to maximize fitness, there are two main possibilities:

1. The environment that this species lives in has given rise to a different approach to the challenge; unusual local factors are altering behaviors on the fringe.
2. The foundations of the behavior are not what we think they are. There are factors not being considered, which are crucial to understanding why these behaviors happen. Just because our model is correct most of the time, doesn't mean the model accurately represents why animals behave the way they do, in this case.

And anyone seriously studying this stuff ought to pause and consider new evidence in this light, if only briefly. In this case, the first option is probably at work. Prairie dogs are mammals, not so different from primates, but as Hoogland states, this is the first evidence of its kind, irrespective of species. Who knows, maybe a re-examination of dispersal behavior in primates will find similar evidence that's been overlooked. If you find it, chances are you'll get it published in Nature or Science.

Hoogland, J. (2013). Prairie Dogs Disperse When All Close Kin Have Disappeared Science, 339 (6124), 1205-1207 DOI: 10.1126/science.1231689

Dispersal Patterns

In this post, I want to discuss an important aspect of primate group behavior: dispersal. Most baboons spend their entire lives as part of a single group, with one main exception. As males approach adulthood, they will disperse, leaving their troop of birth to join a new troop, where they will (usually) spend the rest of their lives.

Female dispersal is rare, for dispersal is hazardous. Leaving the safety of the troop is a problem, but leaving the safety of known territory is also problematic. It's much easier to get away from a predator when you know the location of the closest tree. So why do primates disperse at all? For the most part, dispersal is the only way genes are exchanged between groups of primates. There must be some mechanism for individuals to change groups, or else inbreeding will become a problem.

Male baboons typically leave a troop around the age of 8 or 9. Leaving at that time benefits everyone: the males are strong enough to have a decent chance of surviving on their own (barring bad luck, which happens), the male will have better chances at mating and producing healthy offspring in another troop, and the female relatives of the dispersing male improve their own fitness by encouraging him to leave the troop and reproduce elsewhere.

Females will often refuse to mate with males born in their group, even if the female and male are not directly related. The male can force himself on the female, but that kind of behavior usually isn't worth the extra energy investment. If a male forms a mating pair with a female who doesn't want to be paired with him, she will be looking for any extra-pair copulations she can find, and the male isn't going to get any sympathy from the rest of the troop.

If a male isn't strong enough by age 9? He can usually stick around for a little while longer, but chances are he won't get much stronger, and at some point, the males and females in the troop are likely to let him know that he isn't wanted any longer. In all scenarios, the male will usually become ostracized if he does not leave.

Dispersal is difficult to study. Researchers have to follow young adult males, which is not particularly easy even when they stay within a troop. They need to stay close to the males, so they don't miss when they leave the troop, and then follow them through mostly empty bush, savannah, forest, until they join another troop. Little is known about the daily life of a dispersing male. As far as I am aware, no one has made a career of following dispersing males. Much of what we know has been observed by researchers following troops, who have tried to glean as much as possible from events where new males have joined the troop from outside.

Around the Cape, dispersal is a major issue because the baboons' natural predators have been removed from the ecosystem by humans. While in the process of dispersing, many males are caught by leopards or lions or hyenas. If a male isn't part of a troop, he will more easily fall prey, particularly if he is weak compared to other dispersing males. Without any large predators around, there is a higher male population, and usually not enough space among the existing troops to sustain all of them.

In the second troop, there has been a large influx of males more recently. Bopple seems to be hanging onto his status as alpha, but there have been as many as nine males in a troop of about 50. The troop is almost constantly in chaos. Males need to be able to keep apart from one another, and with that number of males in a single troop, it is simply impossible for them to keep distance between themselves. As a result, they chase each other, they chase the females, and they fight. It isn't a pretty sight. Watching male baboons face-off against each other is exciting, but it does get old, and that sort of volatility doesn't make data collection easy.

For additional reading, and more rigor (though I don't know how outdated their findings are, check out Alberts and Altmann, 1995.

Deadbeat Moms

Why some fathers get left holding the baby.

Scientists have cracked a 140 year old mystery as to why, for some animals, it’s the father rather than the mother that takes care of their young. Researchers from the Universities of Bath, Sheffield and Veszprém (Hungary) found that role reversal was caused by an imbalance in the numbers of males relative to females.

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Another paper published in Nature. This is exciting stuff, as the press articles say, this has been a mystery "140 years old", which is to say, as old as Darwin's work, since it has always been an irrefutable fact that the males of some species do sometimes help rear children. Many researchers have grappled with this problem over the past century and a half. Earlier work tended to appeal to ecological or life history explanations. 

Ecological theories suggest that the physical habitat which the animals inhabit drives males to be involved in the rearing of young. A theoretical example (solely for the sake of discussion): an environment turns dry due to drought, resources are scarce, and if a male and mate succeed in producing live young, the male would be drawn to invest in the infant because the chances of successfully producing more progeny is severely diminished. His energy is better spent helping out. 

Similarly, a life history explanation would suggest that as males age, their ability to compete with other males for mating rights with multiple females decreases. The alternative is to monopolize a female's time, and invest energy is making sure a small number of progeny reach adulthood. While these explanations may seem entirely plausible, the evidence simply does not support these theories.

Until now, thanks to the Liker et al's new theory. In the article's original title, the authors only claim to have answered the question in birds. It may be that no primate species are affected, that is, that role reversals in primates are not caused by an imbalance in sex ratio. Then again, there aren't many primate species in which the male ever takes over rearing for the female.

In many species, the males stick around, but do not get involved. In baboons, the males (and usually fathers) are ever present, but they don't engage in child rearing. They will interact with babies on occasion, but that is a far cry from rearing. Species in which the males play an active role in raising infants: owl monkeys and, of course, humans.

Humans are an interesting case, and not just because all my readers are human. When modern human males take over the rearing of children, is it caused by an imbalance in sex ratio? Probably not.
But then again, humans are not a good study subject for this sort of question; the environments we inhabit are not "ecological". However, our close relatives, chimpanzees and bonobos, do not engage in role reversals (nor do other apes), so the particular type of sexual role reversal we've evolved may be unique.

Liker A, Freckleton RP, & Székely T (2013). The evolution of sex roles in birds is related to adult sex ratio. Nature communications, 4 PMID: 23481395

Lighter Fare

I don't know enough Japanese to understand what the narrator is saying. I'm not even sure what's going on, this doesn't look like a normal mating scene. The monkeys are probably acting weird because they are in a cramped space and the keepers have been trying to get them to mate for hours. There is clearly some creative editing taking place.

Also, these are mandrills, another member of the Papionini Tribe, but they are not baboons. And a final word of warning: this video is NSFW.

Keep It Down

Cheating monkeys try to hide their infidelity

Wild gelada monkeys change their behavior to avoid getting caught cheating on sexual partners. When the dominant leader male in a gelada monkey herd is away, females take up with bachelors, but they're discreet, making fewer sexual noises to avoid detection.

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Original publication is here. I wish that 4 years ago, I'd been aware that this kind of work could get you a paper in Nature (even if the data in this paper have been under collection since 2009). According to the Nature article, geladas engage in extra-pair copulations (ECPs) i.e. when a female has intercourse with a male who she is not paired with. Pairs are usually established by the male following the female around all day and physically preventing any other male from mating with her. So ECP opportunities don't present themselves very often, but then again, there are many hours in the day.

About 10% of gelada copulations are ECPs. The number of ECPs goes up as the distance from the paired male increases, particularly beyond 20 meters. Exactly what you would expect. However, I found the large number of silent copulations surprising. Allow me to digress for a few paragraphs:

One day, I was up on the mountain with the second troop of baboons. The group found their way out of a tall pine forest, into a cultivated field where they could pick grain. Much of the troop was wary of entering the field, probably because the baboons recognized that it was an open, exposed space, which the forest was not. So a large portion of the troop remained in the woods, playing, grooming, socializing.

Bopple, the young and inexperienced alpha male, ventured into the fields. For all of that day, he had been following Nikki, a high ranking female in estrus. Bopple had left her side for this excursion. We were standing at the edge of the forest, so we could watch the animals in the trees as well as those who had stepped into the field to forage.

I heard a female copulation call, which is nothing unusual. But then Bopple came running. He jumped onto a large boulder at the edge of the trees and stared intently at the bushes, from which issued the call, for about a minute. Eventually he relaxed, but stayed up on the boulder, perhaps continuing to keep an eye out. Nikki was nowhere to be seen, for many minutes after.

Nikki engaged in an ECP, and she was smart about it. Bopple didn't take revenge immediately, at least not within a 5 minute window. He might have done so later; he's a male baboon, so beating up on females is a common occurrence. I don't think he could have attacked the offending male, since (as far as anyone knows) there was no information to identify the individual. Displacement aggression would be much more likely.

Geladas are not baboons, even though they are sometimes called "gelada baboons" and are closely related to true baboons. They are part of the same "Tribe" (a non-traditional taxonomic rank that sits between Family and Genus): Papionini. Macaques are also in this Tribe, so the similarities between Species may not be strong. Since doing background research in preparation for this article, the differences between baboons and geladas have never been more apparent to me.

In a previous post, I found an audio sample of a chacma baboon copulation call. Have a listen. Then, watch this video. Copulation calls have been the subject of much study over the years and findings are myriad, but I have never heard baboons copulate as quietly as these geladas. I would not have dreamed this was possible, since it looks like geladas are going through exactly the same behaviors when they mate. According to the Primate Info Network, when in estrus, female geladas usually only mate 2 to 5 times a day. From personal experience and from published evidence, I would be comfortable saying that female chacma baboons copulate at least a hundred times a day.

From this, I infer that the copulatory behaviors of geladas are quite different from those of baboons (or any other species), and if their copulatory behavior is different, odds are that their deceptive behaviors will be different as well. Geladas are a strange species, what with the red swellings on their chests and almost entirely grass based diet. Plus, all gelada vocalizations are quite different from chacma vocalizations, not just copulation calls. I am normally critical of any hypothesis that argues that baboons are the species of choice for studying social mechanism and hominoid evolutionary biology, and since geladas have become a new standard for studying social cognition, I am skeptical of them as well. Compared to baboons, macaques, and apes, we do not know a great deal about gelada cognition. We just haven't been studying geladas for long enough.

le Roux et al have made a good start. This is "the first study to systematically document tactical deception of a primate living in a natural environment", and the importance of that should not be understated. There are two obvious directions to go from here: fill out our understanding of gelada behavior and replicate this research in other species. The first will happen, it is happening in Ethiopia right now, but it will take a while.

The second is more difficult, but in my personal opinion, more important. Unlike the Ethiopian highlands where "there is simply no place to hide", the Bush or Fynbos, the natural habitat of chacmas, affords plenty of opportunities to copulate in secret. Nevertheless, I am all too aware of how difficult study primate concealment behaviors, for readily apparent reasons. I have heard many extra-pair copulations while among the baboons, but I don't know that I have ever seen one. On the other hand, I wasn't looking for them. I don't think it would be exceptionally difficult to do dedicated full-day follows of each monkey in a pair. Someone just has to do it.

le Roux, A., Snyder-Mackler, N., Roberts, E., Beehner, J., & Bergman, T. (2013). Evidence for tactical concealment in a wild primate Nature Communications, 4 DOI: 10.1038/ncomms2468