The Mismeasure of Dog

When you see a study that claims to predict behavior variation with cranial variation your anthropology radar might start pinging. If your anthropology radar's especially sensitive, it will ping regardless of the organism. And when that organism is the domestic dog, you might be tempted to ready the torpedoes before you've even read the abstract.

That's because, for one, people often like to compare human races to dog breeds. Conversations rooted in eugenics or racism often involve judgments of blood purity, much as American Kennel Club members and Westminster Dog Show contestants owe their worthiness to their pure bred ancestors. This isn't a perspective that many anthropologists abide.

And, secondly, there's a long history of measuring human heads, divvying them up by race, showing that they're distinct by race, and then explaining differences in behavior at the race-level in the general or specific context of those race-level differences in the head. Another practice that few anthropologists abide.

We're going to cover some ground on human heads before getting to the dogs'. So please... Sit... Stay... And if you do, we'll get to the dogs in just a second.

Brain size, or cranial capacity, has long been a favorite measure by folks interested in human variation. The cephalic index (CI) has too. These have been used in the name of science by racists, racialists, and folks who are neither. CI might be a favorite because not only does it appear to separate race categories and even populations within them, but it's easily, cheaply, and noninvasively obtained from live humans, while it also avoids phrenological subjectivity.

How phrenology-free is CI? It's not completely clear because, to my knowledge, no one has linked CI to behavior any better than they can with a lumpy left parietal. Remember, however, that many CI uses have not, and are not, for explaining behavior. CI's often measured to study human variation between or within populations, and maybe relatedness, and maybe change over time (evolution).

In anthropology, CI involves the ratio of the breadth to the length of the cranium.

Superior view of a human cranium. Red lines show the two parts of the cephalic index (CI = breadth/length x 100). (photo source)

People even created terms for different CIs: wide, broad skulls are brachycephalic and narrow, long ones are dolicocephalic. CI is influenced greatly by genes (accumulated in ancestry through any number of evolutionary mechanisms). The trait is complex and polygenic, sharing genes that affect other traits. For example, stature is linked to skull length: the taller a person the more dolicocephalic they might be. Environment also contributes to a person's CI which might explain apparent changes at the population-level seen between parents and offspring:

Depicting Franz Boas's CI data collected from 13,000 European-born immigrants and their American-born children in the New York area. (Figure 10.12 from Human Variation: Races, Types, and Ethnic Groups, 6th ed. by Stephen Molnar)

Notice how the changes in the American born children weren't all the same sort of change. That's probably one of the reasons that Corey Sparks and Richard Jantz wrote, "A reassessment of human cranial plasticity: Boas revisited." Boas's big classic dataset had long been used to demonstrate the strength of environmental effects on cranial variation. But with Sparks and Jantz's new consideration of the data, it looks like foreign born and American born people with similar ancestry have more similar head shapes to one another than foreign born compared to American born, regardless of ancestry.

Figure 1 from Sparks and Jantz (2002)

Sparks and Jantz make this point by extending the comparison:

"In America, both Blacks and Whites have experienced significant change in cranial morphology over the past 150 years but have not converged to a common morphology as might be expected if  environmental plasticity plays a major role (29).

We send out our genes wherever our genes may go and that includes, apparently, how our offsprings' adult heads will be shaped, roughly, regardless of where their heads live.

In conclusion, Sparks and Jantz discuss the context a hundred years ago:

"We also must consider the attitude of Boas toward the scientific racism of the day. Evidence of Boas’ disdain for the often typological and racist ideas in anthropology have been reviewed previously (45) and are evident also in his later publications (46–48). Boas’ motives for the immigrant study could have been entwined in his view that the racist and typological nature of early anthropology should end, and his argument for dramatic changes in head form would provide evidence sufficient to cull the typological thinking. We make no claim that Boas made deceptive or ill-contrived conclusions. In
Fig. 1 it is evident that there are differences between American and European-born samples. What we do claim is that when his data are subjected to a modern analysis, they do not support his statements about environmental influence on cranial form."

Acknowledging the strong possibility that genes are more powerful determinants of head shape than environment isn't offensive to many of us today, even those of us who are sensitive about these sorts of data because of their past uses or their potential for future abuses.

But maybe the environment affects different head shape genotypes differently? Why assume that similar environment will result in similar phenotypes if the underlying genotypes are different to start? Isn't the change in phenotype enough to show environment matters enough to consider it important? Perhaps Boas's data aren't sufficient for answering these questions.

And maybe humans just don't have very varied head shapes in the grand scheme of things, in the big picture of whatever "variation" is, and our perception of such typological differences is just what we're good at doing with things like human heads.

But humans and our variation and how we explain and perceive it aren't the main reason we're here today! 

I've introduced human CI, human cranial shape variation in general, and the history of typological race studies linking human head shape and human behavior, because...


One of the main findings of a paper recently published in PLOS ONE is that CI predicts some dog behavior:

link to article

[Now do you see what I meant by my opening paragraph? If not, there's a whole literature out there. Brace's Race is a Four-Letter Word is where you might start.]

For brevity, we're going to ignore the height and weight stuff in this paper and stick to the skull shape parts. But I recommend reading the paper for yourself.

The authors cite some papers to establish that skull shape might be linked to behavior.

One "noted that the morphology of working dogs' heads clustered according to their breed's original purpose. This observation was later supported by a series of studies focused on cephalic index."

"CI is correlated with a tendency for retinal ganglion cells to be concentrated in a form of an area centralis rather than a visual streak. This feature of short-skulled dogs means that they have more visual acuity in the centre of their visual field but less in the periphery."

And this is hypothesized to be linked to their being,

"more likely to follow a human pointing gesture, suggesting that the arrangement of retinal cell may link with aspects of canine social cognition."

Also, they cite a study of dog brain MRIs, linking skull shapes (particularly CI) to,

"progressive pitching of the brains, as well as with a downwards shift in the position of the olfactory lobe." 

This established their premise that differences in head shape reflect differences in brain organization and that,

"CI may be associated with changes in the way dogs perceive stimuli and possibly process information."

It's hard to write this through my insane jealousy, but they traveled to dog shows to collect their metric data. Photographs of the superior view of dogs' heads were taken and then used to measure CI.

They stuck to pure bred animals. Then they looked at a dog behavior survey called C-BARQ to see if CI predicted anything in the same breeds there. The survey's owner-reported, but of course, the author's explicitly acknowledge this source of bias that they can't do anything about (except not use it for science).

And lo and behold, CI predicts a few things:

Self-grooming, chasing, dog-directed aggression, allo-grooming, stranger-directed fear, persistent barking, compulsive staring, stealing food. 

All aren't exactly the kinds of behaviors that have been used to describe human races and populations, but some are.

Anyway, that's not what I really want to talk about. I want to talk about CI and its use for predicting behavior.

Here's how they measured it in the dogs:

Dog CI: "The length was measured from the fingertip to the tip of the nose, and the width was measured from each zygomatic arch, which was displayed by the tape placed around the widest part of the dog's head." (Figure 1 from McGreevy et al., 2014 with my blue lines added)

That's fine as a measure of something like the head. What're you gonna do otherwise at a dog show?

But how's that getting at brain shape? Remember, if the behavior's at all going to be about inbred biology as the premise of the paper sets us up to ask...

That is, if the behavior's not due to conditioning based on how the animal looks to humans and other environmental factors influencing behavioral development which are rightly acknowledged in the paper...

And if changes in behavior during life don't matter (which I don't believe are acknowledged in the paper but is obvious to anyone who's lived with a dog)...

Then we've got to be getting somehow at genes or brain shape or something with CI in order to use it to predict behavior.

But look at what their CI measures:

Boxer cranium with anthropology's CI (left; compare to human at top of post) and with McGreevy et al.'s CI (right). photo source 

Anthropology's CI gets at brain shape much better than McGreevy et al.'s. In fact, their measure isn't getting at brain shape any more than it's getting at meat helmet thickness (all that space between the zygomatic arches and the braincase) and snout length.

With this metric, the paper could be entirely rewritten to discuss not brain shape but meat helmet size as a predictor of behaviors instead.

There are many ways to take this discussion beyond merely pointing out that this measure of brain shape isn't. And I'll wrap-up with a few of those here.

First of all. I'm not an expert on the dog literature but it did stick out that they didn't cite a nice paper in American Naturalist from just a couple years ago--"Large-Scale Diversification of Skull Shape in Domestic Dogs: Disparity and Modularity" by Drake and  Klingenberg--that lends some support to their approach to dog head variation, by breed, and whether it's linked to behavioral variation by breed:

"The amount of shape variation among domestic dogs far exceeds that in wild species, and it is comparable to the disparity throughout the Carnivora. Moreover, domestic dogs occupy a range of novel shapes outside the domain of wild carnivorans."

Look at all the morphospace that dogs' heads are taking up! (from Drake and Klingenberg, 2010)

But Drake and Klingenberg's study also discovers and raises some really important issues that were not considered by McGreevy et al in PLOS ONE:

"The disparity among companion dogs substantially exceeds that of other classes of breeds, suggesting that relaxed functional demands facilitated diversification. Much of the diversity of dog skull shapes stems from variation between short and elongate skulls and from modularity of the face versus that of the neurocranium. These patterns of integration and modularity apply to variation among individuals and breeds, but they also apply to fluctuating asymmetry, indicating they have a shared developmental basis. These patterns of variation are also found for the wolf and across the Carnivora, suggesting that they existed before the domestication of dogs and are not a result of selective breeding."

So we're left wondering why this paper didn't even attempt to deal with genetics and development, that is, the phylogeny of dog breeds. If head shapes vary according to phylogeny, but within those clusters we see variation in behavior, then there's not such a strong link.

I think that phylogeny's ignored because it's not yet worked out. I just went back into the paper and found they do at least bring it up: "A cluster-based analysis of full genomes of these different breeeds may prove helpful in this domain."

It doesn't look like we're very far in dog breed phylogenetics according to (one of my oft go-to pieces for teaching examples of "simple" genetics) Parker, Shearin and Ostrander's review of dog genetics.

"An unsupervised cluster analysis of dogs and wolves. Using clustering algorithms with more than 43,000 single-nucleotide polymorphisms (SNPs), 85 dogs, representing 85 different breeds, along with 43 wolves from Europe and Asia, were assigned to 2–5 populations (inner circle to outer circle, respectively) based solely on genomic content. Each column represents a single individual divided into colors representing genomic populations. Blue indicates a wolf-specific signature, and red indicates a dog-specific signature. Note that the majority of crossover lies between ancient dog breeds and Chinese or Middle Eastern wolves. Figure originally published in Nature (158)." (Figure 1 from Parker et al., 2010)

That's not resolved well enough to be useful for McGreevy et al. (But I could be behind the times.). And granted, the figure I pasted there is aimed at seeing which dogs are most primitive or most like wolves and, maybe then, most like the earliest dogs. But domestic dog breed relatedness must be better worked out than this, given the things Wisdom Panel (using Ostrander's dog breed markers!) can do to pinpoint the breed ancestry of mutts like my pals Elroy and Murphy. (And here's where I learned from the horse's mouth what this test does.)

It does make one wonder, though, whether the dogs that have more wolf-like heads behave more like wolves. That kind of evidence would go a long way to support interest in linking domestic breed heads to their non-wolf-like behavior. But it's not in McGreevy's paper as far as I can tell.

But again, if you've got sensitive anthropoogy radar, it's pinging. First of all, isn't asking about which dogs are most like wolves the same as asking which humans are the most like chimps? Uh, no. But, yeah, kind of. And I'm in no state of mind to expound on that one here today given the trolled-up comment thread that would surely ensue.

But, second, it's troublesome that papers with easy measures and hypothetical (at best) or false (at worst) correlations between anatomy and behavior are published so far in advance of the best sort of data to answer their questions (e.g. a fully resolved phylogeny, let alone mapped genes for the brain shape or the genes for the behavior, etc etc...).

A deterministic and scientifically impatient (to be kind) approach to variation is what still haunts us about the history of physical anthropology. And to see it potentially playing out in other organisms like dogs need not raise any of our politically correct hackles, but I hope it arouses our scientifically critical ones.

The unexamined walk is not worth taking

I've been reading Robert Macfarlane's beautiful book, The Old Ways: A Journey on Foot, about his travels in Britain and beyond, from walks around his home in Cambridge, England, to the bird islands of the north, to ancient seaways where he, no sailor, sails with friends, and on to Spain and even Palestine.  Macfarlane's is a deep, broad, poetic, idiosyncratic and haunting voice and there is much to take in.

His description of his barefoot walks is whimsical (his friend walks barefoot through nettles because it's chili for the feet), his walk across the Broomway, a path in Essex that only when the tide is out, where many a careless wanderer has met his end, shows a bit of a stubborn, defiant nature that I can't help but believe gets him far.  He travels alone, or enlists the aid of wizened sailors or lifelong inhabitants of the moors, he walks with friends.  But he is always observing.

It's an observation that he tosses off when writing of his travels between bird islands in northern Scotland that catches my attention today.  He is sailing from the Isle of Lewis with four experienced sailors on a 75 year old boat, the Jubilee.

I watched gangs of skua pursue single gannets: their method was to fly above a gannet, drop onto its back, force it down onto the sea, smash its skull with their beaks until the gannet was dizzied, then paddle its head underwater with their feet until it vomited up the contents of its stomach, which the skua then ate. 

This is curious indeed and raises many questions.  It's not the most straightforward way to catch fish, after all.  What else do skua eat, and how else do they procure it?  And are they always so brutal?  How on earth could they learn this rather exotic and complex way of dining?

Great Skua; Wikipedia

In my wanderings through what's written about skua, they are most frequently described as "avian pirates."  The fancy word for this is kleptoparasite, but as long as we're anthropomorphizing, "bully" or even "brute" might be more appropriate. Not only do they smash gannets' skulls, but they have been seen to grab them by the wing in mid-flight so that they stall and fall into the sea, whence the poor birds disgorge the fish they've just caught, freeing it for the skua to scavenge.  And it's not just gannets; they also steal from puffins or terns.

Most skua don't always steal what they eat, though.  They do fish themselves, usually splash diving for surface fish, and they often trail fishing boats and scavenge discards or innards.  But they don't live on only fish.  They eat a wide variety of things, including other seabirds; chicks, fledglings and adults, large and small. They also eat eggs, goose barnacles, tons and tons of goose barnacles, and sand eels when they are available, small mammals.

Gannet; Wikipedia

Skua are generalists, omnivores, but individuals also might specialize, preferring sand eels to barnacles, or whitefish to herring. And huge changes in what they eat over time have been documented, so they certainly can adapt to changes in the availability of foods.

Thieves, pirates, kleptoparasites.  Brutes.  Whatever you want to call them, they don't sound like very nice birds.  But are they worse than the gannet, who you might pity given how he is treated by his near-brethren?  The gannet is a hunter, too, hunting fish, that of course it eats alive, often swallowing the poor fish before surfacing after a dive.  And, people on the Isle of Lewis eat gannets, too (though Macfarlane writes: "I know a Lewisian crofter who, when I asked him whether he liked gannet meat, replied, "I gave a piece to the dog and it spent all week licking its arse to take away the taste.")  So we might just be pots calling the kettle black.

It could be, and surely is argued that kleptoparasitic behavior is innate: skua are born to harass gannets.  Not all seabirds treat each other this way, after all, so it must be something in the skua genome that makes them do this.

But, skua aren't only brutes.  Yes, they do treat gannets abominably, and they do dive bomb people who get too close to their nests, which from a person's perspective might seem brutish, but they are doing it to protect their young.  Which means that they do have some warm and fuzzy feelings. Indeed, like other seabirds, skua invest proportionately more in their young than do land birds.

What part of their behavior would be inborn, anyway?  They don't always smash the gannet's skull, they don't always grab their wing, they don't only eat by stealing, they don't only eat fish, indeed their diet can change from year to year, and they aren't always brutes.  So, exactly what kind of protein would a protein-coding gene be coding for to produce this kind of behavior?

Frigate bird; Wikipedia

Perhaps it's something that skua have been teaching their young for millennia, a behavior passed from generation to generation, not inborn at all. But if so, you'd think it might have caught on among other species of seabirds, so everyone would be dive bombing the poor gannet, a particularly skittish bird. Other seabirds are kleptoparasites, most notably the frigate bird, and many will steal another bird's food when the opportunity arises, but the skua version is not a generally shared behavior.  

So, of course what this all brings up is the question of whether there are genes for behavior or not. Or, is behavior an emergent property for which the groundwork is laid by genes that give us all the ability to scavenge and steal, care well for our young, and a whole host of things besides?  If so, we aren't going to find genes 'for' kleptoparasitism, just as we aren't going to find genes for good parenting -- or bad.

Life evolved depending on one creature living on the flesh of another, by and large.  It's a fundamental legacy of our common ancestry; we all share the building blocks of life, and get, or steal, them from others to survive.  No plant or animal likes being eaten alive, often in a cruel way (since other than humans, species haven't got abattoirs that are at least somewhat terror-free and quick in their killing).  It may be cruel for us to maim, kill, or torture one another for reasons other than food, as is so often what humans do.  But killing for food is what we have to do, whether we are eating plants or animals.  This was one of the observations that led Darwin to his theory that adaptations arise via harsh competition.  It's not the only fact of life, but it's a fundamental one.

Are there genes 'for' survival? 

"If sanity and insanity exist, how shall we know them?"

A confluence of events, legal cases, pending legal decisions, journal articles and provocative radio programs this summer naturally lead us here at MT to ask: What is insanity?  What is evil?

The June 30 issue of The Lancet has a piece about the Norwegian Anders Breivik who killed 79 people last summer, asking if he is sane or insane, in fact the only question now before the court as it decides his sentence, as Breivik readily and proudly has claimed credit for the murderous rampage in Norway that shook the world last July.  And he claims as well that he is utterly sane, just a political activist with a point to make.  He was evaluated twice; one psychiatric evaluation found him sane and the other found him insane, diagnosing paranoid schizophrenia with persistent delusions (the questionable existence of the political organization which he claims to be a member of being a case in point).

The fact that psychiatrists do not agree on whether this man is insane, given that they are all dealing with the same man, the same actions and agreement as to who is responsible for them, and the same evidence, is an illustration of the difficulty in defining mental state.  

Both the methods and conclusions of the initial psychiatric report have been widely debated, including by several psychiatrists, after being leaked to the press. Critics said that Breivik's strange word usage, viewed in the first report as neologisms (made-up words or phrases that only have meaning to the speaker and often occur in the speech of people with schizophrenia), were not placed into a relevant right-wing political context. In January, the court decided that Breivik should be involuntarily observed in prison.

Health personnel affiliated with the prison testified in court and reported that they had not seen any signs of psychosis. Neither did the new forensic psychiatrists, Agnar Aspaas and Terje Tørrissen, who concluded that Breivik had dissocial and narcissistic personality disorders with paranoid traits. They believe that the excessive violence on July 22 was the result of extreme political attitudes, and not delusions. Husby and Sørheim think that right-wing extremism is not the defendant's primary issue, but a repository for his delusions. They found that Breivik displayed mental stimulation chiefly when talking about killing and violence.

The outcome of this debate for Breivik will determine whether he is sentenced to prison or to a mental institution for the rest of his life.  For the rest of us, that there can be a debate at all says a lot about the limits of social science, the cultural vs biological determinants of extreme (and not so extreme) behaviors, and how we know the difference, and much more about the sciences that dissect and describe human behaviors and societies.

And of course we've had our own legal drama here at Penn State, the case of Jerry Sandusky and the serial sexual abuse of children.  Is a pedophile insane?  If so, and if it's true that up to a quarter of all boys and a fifth of all girls are sexually abused, and if pedophilia is a form of mental illness, this suggests that a good fraction of the population is mentally ill. 

The constantly evolving DSM, the Diagnostic and Statistical Manual of Mental Disorders, the bible of psychiatric diagnosis, is another case in point.  The fact that it can evolve, that there can be disagreement about diagnoses, and that they can be a moving target speaks volumes about how much psychiatric research can in fact reveal in any objective way.  Indeed, its definitions and inclusions are decided by committees of 'experts' who would not necessarily agree, and while determining whether someone has diabetes or cancer in 1880 or 2012 perhaps hasn't changed that much, by comparison, behavior can be clinically normal sometimes and pathological at others.

Interestingly, these are categories -- affected or not -- and yet we know that behavior is certainly not categorical.  We all probably do some things at some times that some other person might think is too-too-odd to be normal.  And how many people do you have to kill, say, to have crossed from punishably normal to helplessly ill? What kind of science lies behind such treatments of behavior? And here we're not talking about the use many governments make of psychiatric rhetoric to justify imprisoning, sterilizing, or otherwise victimizing people they don't happen to like.  These are very important issues, and raise serious questions to ask of our highly funded social science community.

And indeed none of this is new.  A paper published in Science in 1973, called "On Being Sane in Insane Places",  is a famous and still relevant critique of psychiatric diagnosis. You can hear a quick description of this on the BBC radio program Witness here.  Briefly, Rosenhan wondered if sane people admitted to psychiatric hospitals could be distinguished from the insane context in which they were found.  He had 8 people gain admittance to 12 different hospitals, saying they'd been hearing voices, but then acting completely normal -- that is, sane -- throughout their stay.

Each 'pseudopatient' was diagnosed with schizophrenia, a diagnosis that was never questioned and each was discharged with "schizophrenia, in remission."  Other patients often questioned the diagnosis, telling the pseudopatients that they were clearly sane, or asking if they were professors checking up on the hospital or some such, but the staff never questioned the diagnosis, or declared the person sane.  Granted, hearing voices can be an indication of mental illness, and most people we'd consider sane don't hear voices, so it's no surprise that the fact that the pseudopatients had this on their record did mean something to the staff, and rightly so unless they were to be expected to doubt all reports of symptoms.

But perhaps the more interesting aspect of this story is that once news of this experiment got around, staff at various hospitals asked Rosenhan to challenge them by sending more sane patients.  Many staff members claimed to have identified numerous such patients, when in fact Rosenhan had sent none. 

Rosenhan began his paper thus: "If sanity and insanity exist, how shall we know them?"  Granted, he carried out this experiment before the biologizing of behavior became the norm, at a time when schizophrenia was said to be a "sane response to an insane world" (R.D. Laing) and so on. In fact, in the same paper, 40 years ago, he wrote about it being not uncommon for psychiatrists for the defense in a murder trial to contradict psychiatrists for the prosecution.

Further,

To raise questions regarding normality and abnormality is in no way to question the fact that some behaviors are deviant or odd. Murder is deviant. So, too, are hallucinations. Nor does raising such questions deny the existence of the personal anguish that is often associated with "mental illness."  Anxiety and depression exist. Psychological suffering exists. But normality and abnormality, sanity and insanity, and the diagnoses that flow from them may be less substantive than many believe them to be.

Indeed Rosenhan's question of how we'll know sanity still stands, and we now know that biologizing the answer does not help.

An end of June broadcast, now a podcast of Thinking Allowed on the BBC included a discussion of the sociology of evil.  A question that interested us was whether one must empathize with a killer's motives in order to understand their actions.  That is, do we need to feel Breivik's motives before we can understand why he did what he did?  And thus, before we can determine his sanity?  Would that mean that if we can empathize with his motives we'd consider him sane, and if we can't we'd consider him insane? And do we screen jurors based on their views of this?

The last 40 years have brought the goal of biologizing, including geneticizing behavior -- all behaviors, not just aberrant ones -- as though we can find objective measures of insanity.  So, what does it mean if we can locate a biological explanation for Breivik's actions, if, say, we can determine that his neuronal circuitry went awry?  Say he was unable to empathize with his victims because he was genetically or otherwise mis-wired, would that mean that he can't be held responsible for his actions?

If sanity is not as objective a concept as we like to think, or is socially fluid, then how is it we spend so much effort to find the genes 'for' psychiatric disorders?  Clearly behavior has relation to genetic variation, but just as clearly we have problems on our hands that need to be taken vastly more seriously than they are nowadays.

Science may eventually be able to answer the question of circuitry -- assuming it can define 'normal' -- but the question of assigning responsibility for one's actions, of deciding when a common behavior, such as pedophilia seems to be, is criminal or a psychiatric disorder, whether actions are evil, and whether you do or must feel empathy for them, and so forth are all societal questions that science can't resolve.