Monday, September 23, 2013

Guessing at the mechanisms of dog aggression

I've been thinking a lot lately about how dog aggression works, since the recent dog fighting bust (second largest in history). Fighting dogs are bred for willingness to attack other dogs, but for docility with humans. You don’t want your fighting dog to turn on you in the training yard or in the ring! Willingness to attack another dog, and to continue to attack when the other dog retaliates, is called “gameness.” Despite intense selection on the part of the dog fighters, the dogs show a lot of variation in levels of gameness: some dogs are very game and some are less so, even with training. But it does seem to be true that gameness is heritable, something you can breed for.

So how do you get aggression which is so specific? And what are the fighting dog breeders actually selecting for? What’s different in the DNA of a game dog and a not-game dog? We don’t have any real idea. Recently I came up with one possibility (too new even to be called a theory). It opens more questions than answers, but here’s the story.

There is a well-studied phenomenon in rats and mice related to the position of the fetuses in the uterus. (I know, uterine position is probably not related to genetics, but bear with me for a minute.)  If a female fetus is surrounded by two males, one on each side, she gets more than her usual dose of testosterone in the uterus. Because testosterone helps the developing fetus know what sex to develop into, this extra testosterone makes her develop some masculine characteristics which will stay with her throughout life: she will be what is referred to as a masculinized female. Among other things, her behavior will be affected. Her play style will change to a more rough and tumble style. And she will be more aggressive towards others of her species.

This phenomenon has been demonstrated in multiple species, including guinea pigs, rabbits, and marmots. It is suspected to be in effect in dogs as well: although there are no published papers reporting on it in dogs (at least none that I could find — please let me know if I’m wrong!) I have heard it discussed at dog training seminars as a possibility. And given the range of species it affects and the similarity of effects of reproductive hormones on development across species, it seems really likely to affect dogs.

The big question is: how could this be a genetic phenomenon? The genders of your neighbors in the uterus are random, right? Well, not completely: one of the differences between masculinized and non-masculinized females is that masculinized females have more male offspring. Really. We don't know how that works, though there are some theories about why it may be a useful adaptation to some environments.

Moreover, testosterone doesn't just come from other fetuses. It comes from the mother as well. Some amount of testosterone is normal in development. What if what dog fighters are breeding for, without knowing it, is mothers who produce more testosterone when they are pregnant? Or maybe fetuses which are worse at transforming testosterone into estrogen (as fetuses like to do)? Or fetuses which are more sensitive to testosterone (maybe have more numerous or more sensitive testosterone receptors)?

These questions lead to even more questions, of course, which is why I haven’t even called these ideas a theory yet. Do the more aggressive masculinized female rodents show more aggression to their own species than to humans (which is my initial question about the fighting dogs)? Do male rodents with more males beside them in the uterus show increased levels of aggression? Do we know anything at all about different levels of testosterone released by the dam, not just by uterine neighbors?

There is a lot known about intrauterine position. It is really well studied, partly because it might help us understand the effects of reproductive hormones on fetuses in general, such as possible effects of artificial hormones which are unintentionally introduced into our diets, like BPA. So as I continue to read about it, I hope I’ll start to figure out if this is an idea with legs or just a passing fancy. In the interests of keeping this post readable, I haven’t written about all the interesting facets that I’ve encountered in this phenomenon, so feel free to ask questions. And there are certainly holes in the idea beyond the ones I mentioned, so feel free to point those out, too!

Edited to add: I messed up in suggesting that intra-uterine position might affect dogs the way it has been shown to affect rats, humans, and cattle. Dog placentas are fundamentally different from rat and human placentas, and also different from cow placentas (which form a third category). In short, it would be pretty unlikely for two fetuses to share hormones in-utero in a dog the way they can in rats, humans, and cows. So while I still think it's an interesting idea that a dog fetus could be exposed to different amounts of testosterone in-utero (probably due to processing of hormones by the placenta) and that this could affect its adult behavior, I want to emphasize that it is actually not likely that these hormones could be from other fetuses in a dog. The hormones would be from some difference in the mother, not from a chance alignment of the offspring. So in summary: if your bitch gives birth to one female and two males, that's not a reason to worry about masculinization and temperament in the female.

References
  • Ryan B.C. (2002). Intrauterine position effects, Neuroscience and Behavioral Reviews, 26 (6) 665-678. PMID:
  • Monclus R., Cook T. & Blumstein D.T. (2012). Masculinized female yellow-bellied marmots initiate more social interactions, Biology Letters, 8 (2) 208-210. DOI:
  • Hotchkiss A.K., Lambright C.S., Ostby J.S., Parks-Saldutti L., Vandenbergh J.G. & Gray L.E. (2006). Prenatal Testosterone Exposure Permanently Masculinizes Anogenital Distance, Nipple Development, and Reproductive Tract Morphology in Female Sprague-Dawley Rats, Toxicological Sciences, 96 (2) 335-345. DOI:
  • Bánszegi O., Altbäcker V. & Bilkó Á. (2009). Intrauterine position influences anatomy and behavior in domestic rabbits, Physiology & Behavior, 98 (3) 258-262. DOI:
  • Correa L.A., Frugone M.J. & Soto-Gamboa M. (2013). Social dominance and behavioral consequences of intrauterine position in female groups of the social rodent Octodon degus., Physiology & behavior, PMID:

9 comments:

  1. I want to see some evidence that you can breed for dog aggression and against human aggression. I think that this is mostly a baseless talking point of pit bull apologists. I don't believe that we have such precise tools nor do I believe that anyone breeding for competition would compromise gameness on behalf of this supposed anti-human aggression quality. I see plenty of apologists for all sorts of nasty dogs from a variety of breeds who "manage" and I think that people are willing to manage human aggression while maintaining performance. This happens in many other blood sports, so why do we believe that pit bulls are special?

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    1. It would be really interesting to see some published data on the prevalence of dog aggression vs human aggression in dogs bred and trained to fight. To my knowledge, this doesn't exist, but I can speak to my own personal experience working with a few dozen dogs from such a population. The dogs were uniformly non-aggressive to humans. They varied from extremely sociable and friendly to extremely shy. Only one made me at all nervous to work with; he was highly arousable, but not specifically aggressive. The majority of these dogs were overwhelmingly aggressive to other dogs, although not all of them were.

      I can also say that veterinary behaviorists distinguish in diagnoses between dog aggression and human aggression, and the two diagnoses are commonly separate.

      Working with pit bull type dogs in shelter environments, my experience was different -- some were aggressive to humans, some not, some aggressive to dogs, some not. I can't speak to the breeding or other background of any of these dogs the way I can the population I described above.

      That's my perspective, but as I said, I don't have any published references to back it up, just personal experience!

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    2. It has certainly happened. Alaskan Malamutes for one in the past were quite likely as dog-aggressive and very unlikely as human-aggressive. More recently we've seen the dog-aggression reduced through the breeding.

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  2. Vaguely related, there's this article about birth gender ratios being affected by the earthquake in Japan:

    http://www.newscientist.com/article/mg21929284.900-more-girls-born-in-japan-after-quake-skews-sex-ratio.html#.UkEcXmQ6Ue0

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    1. Interesting, thanks! Stress hormones (glucocorticoids) are closely related to reproductive hormones (come from the same precursors), so this could be caused by a similar mechanism to what I was talking about in my post.

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  3. Related: "freemartin" cows are masculinzed, sterile females caused by having a male twin: http://en.wikipedia.org/wiki/Freemartin

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    1. Yes! Cows have it worse than rodents as cows have more vascular connections between twins than rodents do between littermates. But it is the same thing! Check out my old coverage of freemartins here: http://dogzombie.blogspot.com/2011/01/everything-i-touch-is-missing-uterus-or.html

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  4. Thanks for this post. :) A friend had mentioned this to me. She will not keep a bitch puppy if she had males on either side of her in utero, regardless of how 'nice' the bitch may be (in terms of conformation). However, this is because she believes they'll be 'poor produces' (less fertile) than other bitches.

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    1. She may well be correct. She should warn the new owners about potential behavior issues too!

      I am curious how she knows that there are males on either side since the puppies come out randomly from different horns of the uterus -- maybe just when it is the only female in the litter?

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