Hiatus

I've been quite pleased that I've actually been able to update regularly over the past several months, but things are changing yet again. Starting in September I'm going to be traveling to Scotland to work on a new project, though it will still be in the domain of primate cognition and behavior.

There's no shortage of monkey news and stories to relay, and hopefully I'll have some new stories to tell from this experience. Sooner rather than later, hopefully. For the rest of the summer and into the fall, I'm going to try to update, but it will be sporadic until further notice, i.e. when things settle down and I have an actual schedule figured out.

Conceptions of violence

After last week, I've been catching up with some of Bowles' previous publications and related research. I've read A Cooperative Species, Bowles' masterwork with Herbert Gintis on the origin of altruism and modern society, but reading it once isn't really enough to have read it. It is a dense book filled with math and evidence, theory and data; it requires investiture.

However, Jung-Kyoo Choi and Bowles have included much of their argument in previous publications. It goes like this:

... parochial altruism could have evolved if parochialism promoted intergroup hostilities and the combination of altruism and parochialism contributed to success in these conflicts... under conditions likely to have been experienced by late Pleistocene and early Holocene humans, neither parochialism nor altruism would have been viable singly, but by promoting group conflict, they could have evolved jointly."

As we saw last week, they're leveraging the power of coevolution. But in this case, they're saying that group conflict, or war, as they go on to call it, would have been necessary for human altruism to have evolved. Also, they're effectively promoting group selection, but that's a topic for another time.
 
War is where the problem lies. This is a hot topic, steamy enough for Steven Pinker to rub his hands all over it. However, Steven Pinker's point is that war has decreased since the advent of agriculture. He has very little to say about pre-agricultural violence. Not so for Sex at Dawn, in which the authors' critically examine misconceptions about pre-agricultural life. In short, if early humans weren't violent, then A Cooperative Species' case might be invalid.

Sex at Dawn is a good book. It is thoroughly researched and well written, and one of their big points is that our ancestors are not as violent as they are often made out to be. The book has taken a lot of critical heat, which is not a surprise given the controversial views it espouses. It has many errors (one of which I am about to point out), but I think it has had a positive overall impact on the field. But I'm not here to defend the entire work, so I will discuss a single section.

I want to talk about a chimpanzee example in their chapter on violence. Chimps are not our ancestors, they are cousins, but it is informative to study them when attempting to understand our common origins, what humans used to be like. Chimps are frequently described as violent and aggressive. The best known example of this is Jane Goodall's chimpanzee group in Gombe, Tanzania. Her original study group split in two, and then one part proceeded to violently wipe out the other.

This is not evidence of innate violent tendencies in chimpanzees, says Sex at Dawn, this is merely evidence that human intervention, such as giving chimps food, will cause chimps to alter their behavior and become more aggressive. Same goes for the baboons around Cape Town: the groups with more human contact are more aggressive. They've learned that to get the most out of food hotspots (houses, stores, tourists carrying food), they must act decisively or else another baboon will gobble up all the food. When foraging in the trees for fruits and leaves, there isn't any fighting over food. Those nutrients aren't concentrated enough to be worth fighting over.

However, I must contest this implication by Sex at Dawn. I do not doubt that the Gombe chimpanzees tore themselves apart largely due to human involvement. Yet chimpanzees are routinely violent; they are simply not like their cousins, the bonobos, in this regard. I've heard both John Mitani and David Watts speak about the chimpanzee groups they study in Kibale National Park, Uganda. Mitani was particularly emphatic: these chimpanzees are violent, they fight with each other frequently, and it is not due to human involvement. It is their natural state.

This is hardly a deathblow to Sex at Dawn's argument. We are not chimpanzees; we may have as much (or more) in common with peaceful bonobos as chimps. Plus, this is only part of Sex at Dawn's argument about early human violence. Perhaps more important is the archaeological evidence.

Sex at Dawn points out that many modern scholars, including Pinker, are making their conclusions about early warfare based on sample groups taken from cultures which are not representative of early humans. For instance, the famous yonomamo tribes of South America are from the Amazon, which is a completely different environment from that which our ancestors developed in. Furthermore, the yonomamo aren't even immediate-return hunter-gatherers (like our ancestors were). These errors are not outliers, they are the norm.

A Cooperative Species is better than this. It does not throw caution to the wind and assume that it is acceptable to use modern hunter-gatherer groups as exemplars. It notes that archeological evidence is scarce, and specific evidence of violence even scarcer, and there's not much to be done about that. So it lumps other parts of the world (like Europe and the Americas) into the archaeological sample, and kind of just goes ahead with its story. It feeds in supportive bits of evidence here and there, but this is not the strongest part of the book, and not enough to convince me that war was a foundational part of early human life.

So the case goes to Sex at Dawn, whose points are enough to convince me that early modern humans were not inherently warlike. This is my belief... at least for now.

Agriculture and Property

One of the big questions in the study of ancient human history is, How did agriculture become the main technique humans use to produce food? For thousands if not millions of years, humans gathered food and hunted game to survive; some populations still live this way, as do our surviving ape cousins. To the neophyte, farming might seem like an obvious improvement over hunting and gathering (hereafter, foraging), but it turns out this isn't true. Getting started with agriculture is costly and risky, so how did it happen?

Science has attempted to grapple with this dilemma for decades, and some compelling theories have been developed to grapple with this question. Samuel Bowles' most recent publication in PNAS may be the best original research on the subject in a long time. I'm familiar with Bowles' other work, and I am regularly impressed with the rigor of his models, even if I don't always agree with all of his conclusions. It helps that he is an excellent writer because this isn't the easiest material to make accessible.

In this paper, Bowles and coauthor Jung-Kyuu Choi have built a model, on a foundation of empirical data (archaeological, climatic, and anthropological), which seeks to explain the emergence of agriculture in conjunction with the private property rights. Paleoanthropologists have previously suggested that strict property rights, generally unknown in forager societies, would be necessary for farming to become practical. But, it is difficult to explain why property rights would come into existence because, as with agriculture, there are many disincentives for foragers to adopt property rights. According the authors' model, agriculture and property coevolved: each adaptation is the key to the survival and propagation of the other.

Bowles is an economist by training, so he uses models, agent-based simulations, and game theory to validate his hypothesis. There is a particular brand of game theory called evolutionary game theory which was created to cope with just the sort of questions that Bowles routinely attempts to tackle. The best known evolutionary game theory game is the Hawk Dove game, which demonstrates how two populations of the same species which behave in seemingly irreconcilable ways manage to coexist, in what is known as an Evolutionary Stable Strategy (ESS) situation.

Like so many before them, the authors' adapt the classic Dove Hawk game to fit their needs. Instead of Doves and Hawks, the authors use Sharers, Bourgeois, and Civics. A Sharer's strategy (like a Dove's) is to split a resource by default, but if another individual claims that resource, the Sharer will give all of it up. The Bourgeois is the type that will claim all of resource if possible, contesting if necessary and appropriate (similar to a Hawk). Civics act exactly like Sharers, but if they go up against a Bourgeois, they will band together with other Civics to contest a Bourgeois trying to take the resource. These strategies are modeled on anthropological studies of extant human societies.

Thanks to the power of modern computers and the Monte Carlo engine, the authors can vary other variables as well, such as whether or not property rights are recognized among the populations. If the resource is foraged then ownership is not easily demarcated, and Bourgeois agents will go after it. But if a resource is farmed, then property rights are easily recognized because it is obvious who produced the resource and thus who it belongs to. Bourgeois won't go after these resources; they respect property rights when they are apparent. Additionally, the authors varied climate conditions and simulated inter-group competitions on top of the usual intra-group contests.

After determining all the variables and running the simulations, the authors looked for what combination of conditions create novel ESS situations, with an eye for Bourgeois dominated scenarios since their behavior is the norm for agricultural cultures. A mixed population of Sharers and Bourgeois (but no Civics) forms a steady state, but if you don't have property rights established, Bourgeois have a strong tendency to fight with each other over resources that have no clear owner, which reduces the success of the population. However, if property rights exist, the Bourgeois don't squabble amongst themselves so much, and an all Bourgeois population becomes a stable possibility.

So far the authors have shown that their premises can be incorporated into a model that appears plausible, but does it match the historical facts? A challenge for researchers trying to model early modern human development is matching simulated data with the archaeological record. When we go this far back in time, archaeological evidence is often scarce and difficult to interpret. While agriculture leaves a clear mark on archaeological record, the same is not true for property rights, and there isn't much that anyone can do about that. We just have to make do with what we've got.The authors make do quite nicely. By throwing the Holocene environmental conditions into the mix, they find that

"in the simulations, as in the archaeological record, mixed farming and hunting–gathering is the norm over very long periods, and that the process of transition when it occurred was prolonged, highly varied, and sometimes halting." 

On the other hand,

"the chicken-and-egg problem of farming and private property in our model explains why the transition was a very unlikely event, occurring in only 31 of 1,000 metapopulations that we simulated."

Yet, to me the most striking result is that their model reliably displays the Natufian culture, the first sedentary humans, and possibly the first farmers.

To wrap things up, the authors make some important points about the role of invention in early culture:

"In many histories of technology, the key event is the invention; the subsequent spread occurs inexorably as the result of its superiority in lessening the toil required to sustain life. This model has been suggested for the Holocene revolution; but it does not work. No invention was necessary."

And so, thanks to an agreeable climate, coincident evolution of farming and property right, and well, the human capacity for cultural learning, our ancestors were able to transform from foragers into farmers. Probably. Maybe. We'll have to see what the expert critics have to say in the coming months and years.

This is a great paper. I think that it may have far a reaching influence, so if you're at all interested in the ideas, have a crack at it yourself. It is not terribly long, and quite accessible.

Bowles, S., & Choi, J. (2013). Coevolution of farming and private property during the early Holocene Proceedings of the National Academy of Sciences, 110 (22), 8830-8835 DOI: 10.1073/pnas.1212149110

The Most Unusual Looking Creatures in the World

Several people have recently directed my attention to a set of images floating around the internet, described as "animals you didn't know existed." Its a nice set, but I did know about most of them, even things like the markhor, babirusa, and the dhole (which I only recently discovered). I wrote about the snub-nosed monkey previously; the main reason no one knows about it is because it was only discovered 2.5 years ago.

However, there were plenty of animals I did not recognize. The arthropods on the list are bizarre and were previously unknown to me. Same goes for dolphins on the list. That Irrawaddy fellow is quite a looker. Just what we all needed: a dolphin that appears as creepy as dolphins actually are.

Yet, the most striking animal among the bunch, for me, was the sunda colugo. I thought I'd seen every strange looking primate species there was.

I once spent a long night on Long Street with my colleague, Bellerica. We ended up at Neighborhood, probably my favorite low-key drinking establishment in Cape Town. It was her first time there, and I knew she'd be taken by the collection of old animal books published by Life in (I think) the 60's.

She recognized just about every creatures in those books, or at very least all of the primates. Which was certainly more than I knew. I found myself at a considerable disadvantage, with minimal zoological foundations to rely on. It was an informative experience for me, and she certainly enjoyed the old books and the photos within.

The sunda colugo is often known as the sunda flying lemur, even though it isn't a real lemur. It actually isn't even a real primate, which might explain why I've never heard of them before. They are from the order Dermaptera, which sits alongside order Primates within the mirorder Primatomorpha. Even tarsiers, lemurs, and lorises are primates, even if they're prosimians, and thus not monkeys.

Sunda colugos aren't called "flying lemurs" for nothing. They can glide like flying squirrels, using flaps of skin stretched between their arms and legs. They can soar a hundred meters and lose only ten meters of altitude, turning in the air to control their course all the while. Like many creatures who glide, they spend the majority of their time in the forest canopy, and like many other creatures who live in the canopy, they subsist on leaves, and supplement with other nutritious plant materials they come across.

I am reminded of gibbons, the lesser apes, who also live in this part of the world and spend their lives among the treetops. Gibbons aren't doing very well for themselves these days; most species are endangered, many critically so. Fortunately, colugos have proved adaptable. Their population is not as strong as it has been, but they are doing fine.

Is there really such a thing as a spandrel?

While engaging in a bit of background research for last week's post, I stumbled upon a discussion of spandrels on one of my favorite blogs. When discussing the validity of evolutionary theories and evolutionary psychology in general, spandrels come up fairly often because they are usually red herrings. If a trait is a spandrel, and did not develop in an adaptive way, applying adaptive logic to it in order to justify your theory could undermine your work.

The article I linked to mentions the spandrel of blood color. As far as anyone knows blood doesn't appear red for any adaptive reason, it's just the color imparted by the iron element in hemoglobin. But hold on: the redness of inflamed or swollen tissues is absolutely used adaptively, in primate reproductive swelling, which I can't seem to stop referring back to.

The swellings themselves are certainly not spandrels; in baboons the swellings appear on their rumps, but in geladas swellings appear on their chests. Geladas are perhaps best knows by this trait, having been nicknamed the "bleeding heart baboons" (another of my favorite blogs). In each species the swellings appear in the most visible location. If these traits are adaptive and rely upon the redness of blood, can blood color still be a spandrel?

The real answer is that it doesn't really matter. Adaptive traits and spandrels are all evolving in concert with each other over the course of thousands and millions of years. None of these traits are independent, they are all inexorably intertwined (which is exactly why there are so many adaptive traits that rely on the bright redness of blood function). This is one of the most important lessons of ethology.

Gould and Lewontin, the the creators of the spandrel theory, wished to classify traits as spandrels or not spandrels. Spandrel traits can be found along all avenues of evolutionary biology, not just psychology. For instance, reproductive swellings in primates rely on both biology and psychology. Given the previously discussed risks of misapplying evolutionary psychology, focusing on spandrels just isn't a particularly useful or efficient way for an evolutionary psychologist to spend their time.

Tell Truths, Not Stories

On either side of a recent conference in London, where participants discussed the possibility that "human ancestors were exposed to a period of semiaquatic evolution", a number of voices have taken aim at the so-called Aquatic Ape Hypothesis. The AAH attempts to grapple with some interesting ideas, like why fish protein and fat is so important to our health, notably brain development, or why infants have an instinctual ability to swim, which disappears between 4 and 6 months. According to the mainstream theories of recent human evolution, these facts don't make a whole lot of sense.

It has been pointed out by many journalists (see the infamous Space Ape Hypothesis) that the AAH is still kind of ridiculous. Henry Gee points out the most crucial of flaws in the AAH, and more importantly, faulty underlying reasoning. For instance, sinuses, proposed to aid the theoretical Aquatic Ape in maintaining buoyancy underwater, are found in all mammals.

The AAH debate has been warmed over by a million people, both qualified and unqualified, over the course of decades. We don't need another tiny voice in that mix; I don't have anything to add about the AAH. But, the AAH represents much of what is wrong with evolutionary psychology, and points to a core issue that I've argued and discussed with many of my peers over the past several years: How do you make any progress in evolutionary psychology without creating a bunch of baseless just-so stories?

The short answer is, Slowly, and with a lot of hesitance.

When a psychologist found that that individuals who worry the most about social rejection are most likely to act out in response to rejection cues, what she found was truth. This is a fact of human psychology. There aren't any such facts about ancient psychology because we have no prehistoric psyches to work with, only archaeology, non-human primates, and modern humans.

What can we then say? Still quite a bit. Example: incest avoidance. Animals avoid mating with siblings and other close relatives because of the dangers of incest. There are many mechanisms spread across the kingdom that work to prevent incest from happening; in baboons, males disperse to a new troop to avoid reproducing with their relatives. In humans, we come to recognize those who we grow up in close company with as family members. This frequently applies to childhood friends of the opposite sex, and was a major problem for the sustainability for the Israeli kibbutz system. This is a psychological mechanism, born from an evolutionary need. It is respected enough to have been named. It is called the Westermarck effect.

Ultimately, the validity of evolutionary psychology lies with the validity of all science. If your findings aren't logically sound, other scientists will see through them, and you won't get published. Modern science has an additional tool: statistics, which allows us to falsify theories with varying degrees of confidence. Like any other field, statistics isn't perfected, but it is a powerful tool.

Unless your argument against evolutionary psychology is that all evolutionary psychologists are deranged, there is no particular reason to target evolutionary psychology. Evolutionary psychology is like psychology which is like all of science. There is fraud, there are charlatans, and sometimes just honest people get things wrong. We do what we can about that, but we don't disavow the entire field. 


If you would like to read more about the AAH itself, esteemed professors and bloggers John Hawks and PZ Meyers recommend that you go here. The site is more than just a discussion of the AAH, it is an informative primer for any interested in the logic of evolutionary psychology.

Ruminations on a conversation between primatologists

 A couple years back I had the privilege to hear Robert Sapolsky speak. It was a detailed talk, but given how much I know about his research already, there wasn't a huge amount of new information for me to learn. However, I did pick up on something he only briefly mentioned, and eagerly looked forward to asking him about it after the talk. I said to him:

"The baboons I've seen in the bush are very thin and spend almost all day every day foraging, so they have little time to engage in social interaction except mornings and evenings. You said that your olive baboons have the entire day to socialize; how is this possible?"

Dr. Sapolsky explained that the savanna his baboons live on is a paradise, ripe with easy to find food and moisture. Of course, other baboons could and do live under different conditions. But his baboons were lucky, and their fortune was certainly part of what made them such a great study group.

I haven't thought about this conversation much recently. That is, until I encountered a recent article in National Geographic. In this article, the author asked many of the same questions that came to mind when I heard Sapolsky speak: 'what on earth do these baboons feed on?…and where do they go to drink and sleep?'

Olive baboons are widely spread species in Africa, and while they are known to inhabit arid regions, the Chalbi Desert (the area discussed in this article) is dryer than most other such regions. I am most familiar with baboons sleeping in trees, but in wilder areas where there are more predators (notably leopards), high, steep cliffs are baboons' favored sleeping grounds.

I'm not sure that the authors of the Nat Geo article knew all of this (or much of any of it), but they may have found all the answers they needed, at least for this group of baboons. The troop in question spent a lot of time around doum palm trees, which provide water rich fruit, and shade. Apparently these baboons spend a great deal of the daytime in the doum palms' dense shade. I've seen baboons rest under cover during the heat of the day, but never to the extent found by the authors, in the Chalbi Desert.

These baboons don't live like Sapolsky's monkeys, that is for sure. Their environment does not seem to be able to sustain a large population, but it does seem to be able to support a small one consistently. All this speaks for the remarkable flexibility of baboons. They, like many other species of monkeys; chimpanzees and of course humans, can adapt themselves to survive (and possibly even thrive) in a myriad of different environments. They may not live the most healthy lives, but they will survive to reproduce, and keeps their genes alive.

Oh, and if you were wondering about the truth of Sapolsky story, well have a look at this.

Okay, you probably weren't doubting me, but I'm allowed to be boastful on occasion.

Vervets: the Forbidden Circle

I lied. The second article on vervets did not appear in Science, but in Current Biology. Other than that, I stand by my earlier statement: this is an unusual and thought provoking article, and it happens to be about vervet monkeys.

In this experiment, the authors created a locked container which contained appealing food. The subjects, a troop of vervet monkeys, could see inside and smell the food, but they could not get at it. Only a single low ranking member of the troop was trained in how to open the container.

Without needing to read the paper, I could tell you how things would start out. The dominant individuals in the group would mess around with the container, carrying out all kinds of violent acts in an attempt to force the thing open (which would all fail). Once the alpha got tired of this, it would go do something else and the second rank individual would make similar attempts to open the container. This is a common scene among the baboons, when they're trying to get into a locked storeroom or car.

In order for the monkeys to get at and eat the food inside the container, all dominant individuals would need to exhaust their own interest and wait. They were also required to stay a safe distance away from the container, somewhere between 10 and 15 meters. Only when the dominant individuals were a safe distance away would the monkey trained to open the container actually open the container.

It took most of these troops a few long trials to begin to understand that they would need to show restraint. But after they picked up this notion, the process went surprisingly smoothly and quickly, and the trained monkey would invariably be allowed to open the container. Unsurprisingly, the subject group that was experienced in raiding garbage bins and picnics took much longer to get over the fact that only a single low ranked individual could open the container. The authors go into great deal of game theory, but I will leave that by the wayside and get to the conclusions.

There are a number of fairly impressive accomplishments included in this paper. First, that the authors were able to train a wild vervet, to essentially be a confidant in their experiment. It is kind of incredible. Second, their main results show that these monkeys are capable of restraint on group and individual levels. Monkeys are notoriously bad at self-control, but this shows the power of reinforcement learning. I can't imagine any of the monkeys I've worked with, in captivity or the wild, being trained to show these levels of restraint. So kudos to the authors, and kudos to vervet monkeys.

Vervets: Flavor & Social Transmission

This week is vervet week. I have declared it. Coming from me, this means a lot, since I've never been particularly interested in vervet monkeys. But, two articles have been released in science recently: both on vervets, both so intriguing that I have been compulsively rereading them.

The first of these comes from Andy Whiten of primate culture fame. He has done impressive work in the past, and this latest vervet paper is an extension of that, though perhaps not the intuitive extension. The authors presented their wild vervet subjects with two types of food, varying two attributes of each type. First, the food was either colored blue or pink. Second, the food either tasted good, or tasted terrible.

Taste aversion can be found in pretty much all mammals; a type of learning that most humans are familiar with. By taste aversion, I mean that when you taste something bad you learn very quickly not to eat it again. Often it only takes one exposure to learn this, which in the animal behavior world is very very fast. Not only will animals learn to avoid foods that taste digusting, but they will also learn to avoid foods that they think made them sick, even if they didn't eat anything that tasted bad.

There is a broad literature on taste aversion in rats (a literature I happen to know pretty well), and in rats you will find even stranger, related phenomena. Rats possess the ability to socially transmit taste preferences through their sense of smell. They will actually smell the breath of other rats, and later, they will show a preference for food that smells and tastes like the odors they smelled on the other rat.

It turns out that vervets can do basically the same thing. The authors of this paper have shown that while vervets quickly learn to avoid the color of food that they know tastes bad, they can learn socially through watching other vervets to ignore their earlier preferences. For example, if a male vervet learns that pink food tastes gross, and then the male disperses to another group where everyone learned a long time ago that blue food doesn't taste good, the newcomer male will watch and learn to eat blue food, in spite of his earlier memories.

Rats possess a unique neurochemical mechanism for learning this kind of stuff, and cannot learn taste preferences socially. Yet this is exactly what vervets do: watch other members of their own species and using that information, learn new preferences and extinguish old ones.

To see this in vervets is striking. If someone reported these results in chimpanzees, it would not be particularly surprising because chimps are extremely smart and adaptive. Vervets are not great apes, not lesser apes, they're just old world monkeys whose brains are smaller than many other old world monkeys, notably macaques and baboons. If we see this kind of behavior in vervets, it really does suggest that this cognitive ability is fundamental in all old world monkeys.

Moreover, the authors refer to this type of learning as "cultural learning". I am not sure if I fully agree with this; the line between cultural and social learning is not clear. However, I would certainly say that this type of learning is at least an evolutionary antecedent to cultural learning.

van de Waal, E., Borgeaud, C., & Whiten, A. (2013). Potent Social Learning and Conformity Shape a Wild Primate's Foraging Decisions Science, 340 (6131), 483-485 DOI: 10.1126/science.1232769

Lip smacking and the origins of language

In a previous installment, I discussed gelada vocalizations and some new research specifically dealing with copulation calls. Thore Bergman, one of the same researchers who put together that paper, just published a short correspondence discussing a wide array of gelada vocalizations and their relationship to the evolution of human language.

This topic is been a tricky subject to approach because no primates' vocal range compares to humans'. The closest connection has been "lipsmacking", which is exactly what it sounds like: monkeys smacking their lips at each other without vocalizing. It very common among multitude of primate species.

Lipsmacking isn't a behavior that intuitively seems like it would have a connection to human language, but it turns out that the rate at which these monkeys smack their lips together is remarkably similar to the rate at which human lips open and close when they produce speech.

Gelada's take lipsmacking a step further. It turns out that they can produce a vocalization while smacking their lips together; it is called a "wobble". A as with lipsmacks, the rhythm of these wobbles is very close to the rhythm of human speech (between 3 and 8 Hz).

As I am fond of repeating, wobbles and human language are an example of convergent evolution. Baboons don't wobble. Chimps don't wobble. All of these species lipsmack. Even though the wobble is closer to language than the lipsmack, we just aren't that closely related to geladas, so the simplest explanation is that wobbles and language evolved independently from the same foundation, lipsmacking.

Have a look for yourself. Bergman provided a video in the supplement to his new publication, here.

Monkey Funk (or lack thereof)

Sea lion is first non-human animal to keep a beat

Ronan is the first known non-human mammal successfully trained to bob her head in time with a metronome-like sound — and then to apply her new skill to tempos and music she had not previously heard, according to researchers at the Long Marine Laboratory at the University of California, Santa Cruz.

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This is the biggest news in auditory (or at least musical) animal behavior, right now. Make sure you get to the bottom of the linked page where you will be rewarded with video evidence. It will be worth your while.

Reminds me of a similar, recent article featuring rhesus macaques. I was quite surprised to find that I had not previously written a post about said article. I won't let it by me a second time.

In this article, the authors describe results which suggest that macaques can detect rhythmic perception, but not beat induction (according to the earlier study, sea lions are the only mammal other than humans that can do both). The theory that there is a distinction between these two faculties is know as the dissociation hypothesis.

None of these terms are intuitively obvious. Beat induction is the ability to detect regularity of beats in a rhythm. It is what gives us our ability to tap our foot along with the beat in a song. Rhythmic perception merely refers to the ability to tell that some specific amount of time has passed. This sort of timing work has been studied extensively in many animal species, and it is well known that pretty much all mammals can time intervals. In fact, I have myself done some work demonstrating rhesus macaques' flexibility in timing intervals (Diapadion et al, unpublished results or something).

There is a major drawback to this monkey study: there is no behavioral data. It is entirely EEG. In many ways, I prefer EEG to fMRI or electrophysiology for brain imaging. EEG takes a distributed look at the activity of billions of neurons, unlike eletrophysiology, where you isolate signals from single neurons and pretend that the entire brain region surrounding acts the same way. fMRI also takes a distributed look at brain activity; in fact it is often more accurate than EEG. Unfortunately you can't put monkey into a MRI scanner unless the monkey has been knocked unconscious. You have to stay still in the scanner to get good data, and monkeys, well, they're not so good at that, ever.

fMRI is also superior to EEG because fMRI allows you to see deep into the brain, whereas EEG only lets you look at surface areas because it is on the surface of the skull that you place the EEG electrodes. There might be something going on deep in the auditory cortices that the authors' EEG findings are missing. Which is why it would be nice to see some results from additional metrics. Practically speaking, I don't believe it is likely that the authors are mistaken; the primate literature supports their hypothesis.

In the sea lion video, the speaker suggests that beat keeping may be far more widespread in the animal kingdom than previously thought. No, probably not. This EEG study suggests that monkeys are totally incapable of beat induction, and it stands to reason (and evidence) that this holds for other primates. As it stands, convergent evolution is the most likely explanation.

Honing, H., Merchant, H., Háden, G., Prado, L., & Bartolo, R. (2012). Rhesus Monkeys (Macaca mulatta) Detect Rhythmic Groups in Music, but Not the Beat PLoS ONE, 7 (12) DOI: 10.1371/journal.pone.0051369

Old Drifters

Since reading and writing about prairie dog dispersal, my thoughts have returned to some odd events which took place among the baboons some time ago.

I wrote about these occurrences in a some old posts. To summarize: two old male baboons, Chester and Mortimer, both moved from the main troop to the second troop, higher up on the mountain. In Chester's case, he was following Eunice, his favorite female. Mortimer's motives were less clear. Eventually, both returned to the main troop. This was not the first time the older males have pulled stunts like this, and it won't be the last. Although, there won't be many more opportunities for these two in particular. They're getting pretty old.

At the time, I wondered if there were any examples of behavior like this in the literature. The prairie dog article sheds some fresh light on these baboons' behavior. I don't think these baboons are dispersing for the same reason as prairie dogs, but I think it is likely that mid to late-life dispersal may be more common, and perhaps systematic, than researchers have been inclined to believe.

For my baboons, the odd origin of these troops (they were all one big troop many years ago when the population was smaller) muddies the water. These behaviors might not even be valid dispersals. However, it is difficult to say if these males would leave the area if they had the option, for baboons in Tokai can't disperse beyond the forest without encountering serious resistance from human populations. Or, as I am fond of considering, they might just be outliers.

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

They All Look The Same

A few weeks have passed since Iran claimed to have sent a monkey to space and back. It did not take long for skeptics to point out that the two monkeys look nothing alike. I can't begin to explain why Iran wouldn't do a better job staging their publicity photographs. My mind has been occupied with (in my opinion) a more interesting question: Why is it easy to distinguish between individuals of some primate species, but not others?

I've spent time with a number of primate species, but in terms of sheer hours of exposure, chacma baboons and rhesus macaques take the top two slots. I know both these species very well. Yet, rhesus macaques are easy for me to distinguish between, while chacma baboons are exceptionally difficult to identify. After spending a few hours with some macaques, I can reliably tell you their name and personality, mostly from looking at their faces. After spending hundreds of hours with the same baboons, I could not tell them apart, at least not based on their faces. They really do all look the same. Its more effective to look at the pattern of tears on their ears, and the shape of the callosities on their rumps. Its quite humbling, actually.

A similar phenomena exists in humans, known as the Cross-Race Effect. Or, as the All Look Same effect. In humans, the difference is based on race, but its not racism. How much of the effect can be explained by nature versus nurture is a matter of contention, but has everything to do with an individual's upbringing, who the individual spends time around as they grow up.

The monkey face recognition effect must be different because I didn't grow up spending large amounts of time around rhesus monkeys. So, I turned to genetic diversity for ideas. The more diverse a species is, the easier it should be to identify within the species. It stands to reason that the species which is much easier to identify (rhesus macaques) would have higher genetic diversity.

Research started off easy. The rhesus macaque is three times as diverse but more closely equivalent in damaging coding variation as compared to the human. That is about as straight forward an answer as I have ever seen in the title of an academic publication. Okay, so what about chacma baboons?

Baboon diversity is not as well understood. Rhesus monkeys are widespread, plus they're the animal of choice when it comes to biomedical research. Baboons are also widespread, and favorites of field researchers. But you don't see them as much in labs, so genetic testing is not a routine procedure. Nonetheless, I found an article which addresses my questions.

Quantifying diversity is a not a simple matter. From data collection to bio-informatic analysis, it can be a bumpy road. I don't know why exactly Newman et al. chose to quantify diversity with the mean percent pairwise difference in haplotypes, but it happens to be pretty easy to explain. To use the metric, you take your data, a set of DNA samples from individual monkeys, and compare each individual's DNA to everyone else's within the same species. You count the number of differences  observed between individual base pairs at the same places in the DNA sequences. Then, convert that number into a percentage, and finally, average all of the comparisons between individuals. That's the author's measure of within species diversity.

The diversity found in rhesus macaques was 4.2%. In chacma baboons, it was 0.9%. That is a considerable difference. These numbers are only given a small mention in this part of the paper, so I don't know the margins of error. Nevertheless, these finding support the hypothesis that baboons are harder to distinguish because there is really is less distinguishing information available; less diversity within the species.

However, there are some extenuating circumstances. The baboons I interact with in Cape Town are from a small population, in fact, a subspecies of chacma baboon, Papio ursinus ursinus. Now their diversity is cut down even further, possibly by an order of magnitude or more.

Most of the rhesus macaques I've spent time with were in captive colonies. There are many rhesus sub-species; no one knows the pedigree of colony monkeys, another dirty secret of the biomedical community. But, my best guess is that they came from rhesus populations as wide spread as you can imagine, so the diversity in colonies is likely to approach 4.2%. I have interacted with wild groups of rhesus macaques, but only for short periods (hours), not for months as I have with the baboons. Are they more difficult to identify than the captive monkeys I know? Yes, they are, but not as difficult as wild baboons.

Which raises a follow-up question: What is the right way to quantify how easy it is to tell members of a species or sub-species apart? My gut feelings aren't going to hold up under scrutiny. Appropriate paradigms already exist: show people (or monkeys) a series of faces, some new some repeated, and ask them if they've seen each one before. As I've heard many Professors say (to myself and others around me), "you could get a thesis out of these experiments."

Yuan, Q., Zhou, Z., Lindell, S., Higley, J., Ferguson, B., Thompson, R., Lopez, J., Suomi, S., Baghal, B., Baker, M., Mash, D., Barr, C., & Goldman, D. (2012). The rhesus macaque is three times as diverse but more closely equivalent in damaging coding variation as compared to the human BMC Genetics, 13 (1) DOI: 10.1186/1471-2156-13-52
Newman, T., Jolly, C., & Rogers, J. (2004). Mitochondrial phylogeny and systematics of baboons (Papio) American Journal of Physical Anthropology, 124 (1), 17-27 DOI: 10.1002/ajpa.10340