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: 12479841
• Monclus R., Cook T. & Blumstein D.T. (2012). Masculinized female yellow-bellied marmots initiate more social interactions, Biology Letters, 8 (2) 208-210. DOI: 10.1098/rsbl.2011.0754
• 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: 10.1093/toxsci/kfm002
• Bánszegi O., Altbäcker V. & Bilkó Á. (2009). Intrauterine position influences anatomy and behavior in domestic rabbits, Physiology & Behavior, 98 (3) 258-262. DOI: 10.1016/j.physbeh.2009.05.016
• 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: 23769692

He’s a lover, not a fighter: outreach for the prevention of dog fighting

[This is the presentation I gave at a shelter staff meeting this week, as part of my shelter medicine externship.]

How can we redirect inner city kids away from using their pit bulls for dog fighting, and towards other activities? I looked into two programs that exist to reach out to youth and do exactly that. These programs focus on prevention of dog fighting, on educating kids before they decide that dog fighting is cool, rather than focusing on the punishment of dog fighters.

The first program I looked at is the End Dogfighting campaign from the Humane Society of the United States. The End Dogfighting campaign has several different arms:

• The Pit Bull Training Team provides alternative activities for youths with pit bulls (or, presumably, other breeds). Set up as a weekly class, the PBTT introduces kids to obedience and agility, and also provides some socialization for the dogs (since fighting dogs, obviously, often have poor social skills with other dogs). For students who do well and stick it out to the end, there is a Canine Good Citizen (CGC) test that they can take. If they pass, they receive a CGC title for their dog from the AKC, certifying that they have a well trained dog. Graduates of the class are encouraged to stick around and mentor new students.
• The Humane Education arm of the campaign is an 8 week curriculum for middle school students. It’s intended to be a fun set of classes, with mock game shows, videos, and hands on projects. The message of the class is that dog fighting is a crime, it’s violent, and it’s animal cruelty.
• The First Responder Outreach arm of the campaign is aimed at postal workers, utility works, and public works employees — the people who are out in the neighborhood who might encounter signs of dog fighting rings. The HSUS provides posters with information about what to look for, such as how to recognize the fighting pit where dog fights occur. The HSUS may also provide a presentation if asked.
• The Law Enforcement Outreach arm of the campaign provides a $5,000 reward for tips leading to the conviction of a dog fighter; law enforcement training classes; a database with the names of known dog fighters; grants for handling seized animals (controversial, as the HSUS recommends that such animals be immediately euthanized); and prosecutor training.

The End Dogfighting Campaign began in 2006 in Chicago. Since then it has expanded to Atlanta and Philadelphia. So far, the campaign is focused on big cities. It seems unlikely that we’re next on their list. However, the HSUS freely provides materials for download to let other groups try to implement individual arms of the campaign.

I also looked into the Lug Nuts program, which is informal weight pulling contests in cities with dog fighting problems — again, providing alternative activities for people to do with their pit bulls. In a Lug Nuts contest, children’s sleds are loaded with food until they are very heavy. Dogs (not always pit bulls, although pits are very muscular and tend to be very strong dogs) are hooked to the sleds with special harnesses. The dog that pulls the farthest wins. The food can also serve as a prize, and the prize can be doubled for animals who are spayed or neutered. As the web page for the program says, there is excitement! Machismo! Thrill! The competitive aspect of Lug Nuts may be an important way to draw people in.

Sue Sternberg started Lug Nuts in New Haven in 2002. It is associated with a Training Wheels program, which brings pet supplies and veterinary services into underserved areas, and takes the opportunity to also bring some education about positive reinforcement training to dog owners.

So who should be going into inner city communities and telling people about these programs to change how they interact with their dogs? I am pretty sure that if I tried, I’d get laughed at. The End Dogfighting campaign solved this problem with the creation of Anti-Dogfighting Advocates (ADAs), graduated students from the program. They encourage people to come in to the weekly classes, and check in on them during the week to keep their interest up. There is definitely a bootstrapping problem here. Who goes out and convinces people to go to the first classes? But the approach of keeping community members involved even after graduation is a nice one.

I like the positive approaches of these two programs. Positive reinforcement works better than punishment! I’d love to see both programs expand to more cities.