The vegetables of genetics

Today I’m working on revisions for my DNA class at IAABC, which starts Monday, April 24. This will be the second time I’ve offered this class; it’s the first in a series of four classes (which you can take in any order, so this one isn’t required for later classes). And the auditor’s price is still super low to encourage people to take it just for fun.

I’m never sure how to promote this class. Will it offer you direct insights into how to modify behavior? It won’t, of course. It will tell you what DNA is and what genes are and how at a low level DNA differences affect traits. For how to apply this stuff to behavior consulting, you should refer to the fourth class in the series, which is about behavioral genetics.

But while the fourth class has that stuff we all want to know in it, to really understand how all that stuff works you really want to take this first class. Sometimes I think of this one as the vegetables class: you have to eat your veggies before you can have your dessert. But I hope it’s not just because I’m a genetics geek that I do think this class has some fascinating material in its own right. It’s not overcooked frozen peas, it’s heirloom tomatoes from the farmer's market. In later classes I’ll talk about the weird ways our DNA can affect our personalities, and in order to deeply understand what I mean, you want to know how DNA is put together and how the body reads the genetic code and how things can go wrong.

And by the way, I make sure all of my classes have something in them for everyone, so if you are a genetics geek too, come take the class for the optional resources, which have loads of articles with new research findings in which we (surprise!) realize DNA is more complicated than we at first thought, and getting more complicated the closer we look at it.

And if anyone can help me explain how to market this funny little class and explain to people that this really is stuff it’s good to know (for behavior consulting but also just for life in the middle of the Genomics Revolution) then please tell me!

Puppies and Pointing

Why are some dogs better at paying attention to humans, particularly human gestures like pointing, than others? We know genetics has something to do with it, because some breeds (like border collies) are a lot better at responding to human signals than others like beagles. To better understand the biology driving differences in ability to respond to human signals, researchers at the Family Dog Project compared dogs and wolves as they grew up. They knew that wolves can respond to human signals, but that they are better at this when they have been extensively socialized, whereas dogs can understand human signals with much less socialization. But at what age do these differences manifest?

Image from the Family Dog Project

The researchers used a pointing test to measure ability to respond to human signals. This test has been used on dogs before: if a dog is given a choice of two bowls, only one of which contains food, and he can't see where the food is, will he follow a person's pointing gesture to pick the right bowl? (The bowl with no food in it is rubbed with food so the dogs can't use their noses to get the right answer.) This test has been done in the past with dogs versus human children (dogs do about the same as two year old kids on this task), dogs versus wolves (dogs generally outperform wolves, unless the wolves have a whole lot of experience with humans), and dogs versus chimpanzees, our closest primate relatives (dogs outperform chimps!).

For this study, the researchers compared hand-reared (i.e., well socialized) 8-week old dog and wolf puppies; 4 month old dog and wolf puppies; and adult dogs and wolves. They tested the animals' abilities both with "proximal" pointing (putting their finger right up to the bowl) and "distal" pointing (standing farther away and indicating the bowl) - except that, since very young puppies and wolves don't see well, they didn't test the distal pointing in the 8 week old babies. What they found:

• The 8 week old puppies (dogs and wolves) had similar ability to follow the proximal pointing gesture with the researcher's finger right next to the bowl. However, 6 of the 13 wolf puppies tested had to be removed from the trial because they couldn't be held on the start line or didn't go choose a bowl. Of the 9 puppies, only one was removed for similar reasons.
  
• 4 month old dogs did better at distal pointing (with the researcher standing away from the bowl and indicating it) than 4 month old wolves did. In fact, the 4 month old wolves seemed to do no better than chance.
  
• Adult dogs and wolves did equally well with both proximal and distal pointing.
  
• At all three ages, wolves needed more time to establish eye contact with the pointing human than dogs did.

So all the animals at all ages were able to understand a pointing gesture when the human put their hand right up to the bowl. But pointing from farther away was harder, as you'd expect. Very young puppies (dog and wolf) were not tested on that task. At four months, wolves hadn't figured it out yet, but dogs had. As adults, the wolves had caught up. These were highly socialized adult wolves with a great deal of experience with humans.

It's interesting that dogs seem to develop the ability to understand a more difficult human pointing gesture at a younger age than wolves - and particularly interesting that this may have to do with the fact that wolves are not as eager to look us in the eye as dogs are. (If you don't look at someone, it's hard to follow their pointing gesture!)

So what does this mean for differences in different dog breeds? Do different dog breeds have differences in the timing of their cognitive development? Does this affect how much attention they pay to us, and perhaps how easy they are to train? We don't know, but I think this is one direction dog research needs to go.

(By the way, check out the original paper - it's open access, and has some great videos of dog and wolf puppies at the end!)

Gácsi, Márta, et al. "Explaining dog wolf differences in utilizing human pointing gestures: selection for synergistic shifts in the development of some social skills." PLoS One 4.8 (2009): e6584.

This post was originally published with slight modifications at Darwin's Dogs.

Puppies and dog breeds

Thanks to Julie Wurth for a great interview with me and Linda Case of The Science Dog in our local paper, the News-Gazette.

Since the article was about getting a new puppy and provided pointers to this blog I figured it was a good idea to suggest some old posts to any new readers. As always, for a constant stream of interesting dog science articles not written by me, follow me on Twitter or like my page on Facebook!

• The Replacement Dog: how a veterinarian / dog rescuer / geneticist searched for the right puppy

• The history of dog breeds: Victorians, genetics, and the importance of diversity

And an update on Dash - he is turning into a fine young man. Here he is from a few days ago.

Dashiell, aged six months

Training the dog in front of me

It's been hard to train two dogs at once. My old dog, Jack, never minded when I trained my young dog, Jenny. He was happy to chill out on the couch. But Jenny is different now that she's the old dog and Dash is the young dog: she wants to be part of whatever I'm doing, especially if it involves food. If I baby-gate her in another room while I train the puppy (and puppies take a lot of training) then she will sit right up against the gate and obsess. (Up side: gates have become much less scary to her recently, even though they are just as likely as they always were to fall down and go boom.) When I try to put her upstairs, she goes reluctantly and is ramped up and anxious when I let her out.

I read "A Secret to Training Two Dogs" by Eileen And Dogs, and determined that I would use mat training. I'd been told time and again that I should be mat training Jenny anyways: take the mat to the scary new place, and you have a safe haven for your shy dog. (Jenny is still extremely shy, though hugely improved from when I got her.)

I got a Mutt Matt for Dash and pulled a tiny old area rug out of storage for Jenny. Dash picked up the mat concept quickly: you lie down on it and get treats. In fact I now have trouble prying him off of it to put it away.

Dash on his mat.

But Jenny couldn't seem to do it. She eventually learned to lie down on her mat, but didn't like to stay on it. I tried asking them both to stay on their mats while I walked around them: Dash was glued to his, but Jenny would come off of hers and wander away.

This morning I unrolled Dash's mat and asked him to go to it, and Jenny went and hopped on the couch. The light bulb went off: this is my dog who refused to touch foot to ground unless absolutely necessary for the first months I had her. She lived on couches. I had to train her to get off of them. I used target practice with a yogurt lid that I moved farther and farther from the couch; she came up with the solution of picking the lid up and putting it back on the couch so she could keep getting rewarded without having to leave her safe space. The first time I saw her sleeping on the floor, four years after coming to live with me, I almost cried from joy. She even already has a "go to your couch" command which is quite strong.

Jenny training on her couch, shortly after she came to live with me.

So I trained Dash while she was on her couch, and then trained her while Dash was on his mat, and it was lovely. Both dogs were stuck in place until I asked them to get off. I was able to train something fun (a tunnel) working one dog at a time (with frequent treats thrown to the other).

The moral, as Denise Fenzi tells us in her excellent blog post, is to Train the Dog in Front of You. See what works for her, not what you think should work for all dogs.

Which leaves me to figure out how I will take a couch with me to the next strange place I need to bring Jenny...

Jenny on her couch two years ago.

The Replacement Dog: how a veterinarian / dog rescuer / geneticist searched for the right puppy

The death of my fifteen year old golden retriever Jack wasn’t just about my loss. It was about finding someone else to do his job, which for the last five years had been serving as a security blanket for Jenny, my shy collie mix. Jenny depended on him to tell her when people did not intend to eat her, to run interference with well-meaning strangers, and to demonstrate calm at the veterinary clinic. We could not remain a single dog household for long.

Jack and Jenny

I adopted Jenny at age 13 months. She had never been off the farm where she was born until her surrender to a shelter, and the world proved much larger than she expected. Jenny has excellent dog skills but a crippling anxiety upon encountering new people or environments. I adopted her knowing about her idiosyncrasies because I wanted to study anxiety in dogs, and wanted to experience it first hand. And so I have; living with Jenny has informed my understanding of anxiety in a way that reading about it never could have.

In my research, studying the way genetics and environment interact to affect the risk of anxiety has brought me back time and again to the importance of early environment: in utero environment, early maternal care, and puppy socialization. How the brain changes during and after the socialization period turns out to be a huge part of my research interests, and to learn from the source as I had done with Jenny, I would need a puppy, and a very young one at that. I’ve only adopted adult dogs in the past, but now is an excellent time for me to raise a puppy, as I work from home many days.

A puppy who would grow up to fit in well with Jenny had to fit a specific mold: confident around people and other dogs, but not so pushy as to annoy her. Someone she could play with. Someone male, because I didn’t want to deal with girl dog politics for the next ten years.

Jenny

Now, I have counseled others that adopting a very young mixed breed puppy from a shelter or rescue group means you really have no idea at all who you have just brought home, and that there is no shame in purchasing a dog from a responsible breeder. However, in practice, I balked at purchasing a dog. I completed an intense shelter medicine internship at the University of Florida several years ago, and I still feel part of that community. As the distance between the present day and that experience increases, I find myself holding tighter to those connections and looking for new ways to remain a part of sheltering. Purchasing a dog who was not going to be in want of a home felt a bit like eating humanely raised meat: I tell myself it’s okay for others to do it, but when I actually try to do it myself, some part of me rebels.

Yet as I looked at puppies from local rescue groups, in short order I found myself in a panic: could I really adopt a puppy whose genetics were completely unknown, whose parents I most likely couldn’t meet, and who had almost certainly had some early life trauma before ending up in foster care? Genetics and early experience are both critical in shaping the adult personality, and while I hope I could handle dealing with another shy dog, Jenny needed someone dependable, not another neurotic failing to keep it together when the mailman drove past.

When I started to seriously consider purchasing a dog, I had to decide on a breed. I love retriever-collie mixes: ideally the best of both worlds, retriever-social and collie-smart. But finding a responsible breeder of retriever-collie mixes seemed a tall order. Border collies are too intense for me. Australian shepherds have their tails docked so short. And I wanted to find a breed that is not recognized by the AKC, that is absolutely not bred for looks, that possibly even has open stud books to keep the genetics pool large and diverse.

I found the Scotch Collie and the English Shepherd. The Scotch Collie club had an open stud book policy going for it (good for them!). The English Shepherd club had a closed stud book policy (open it up, guys!) but it had been open relatively recently, the breed isn’t recognized by the AKC, and the dogs can’t be shown in conformation classes. The breed is a versatile working breed. Both breeds have lovely breed standards that accept a wide range of phenotypes (for example, 30-80 lbs in adult weight - a wide range!), which in itself tells the story of breeding for temperament and not looks.

In the end, I chose the English Shepherd based on the fact that there are more of them around, so it was easier to find a litter promptly. Waiting a few months would mean potty training a puppy in January in the Midwest, an experience I’ll leave to others.

The English Shepherd club maintained a list of breeders who had available puppies, with lots of information about the parents. It’s a well designed resource, and I link to it not to encourage others to run out and get an ES puppy (they are smart and high energy and not for everyone) but to provide an example of what kinds of information should be provided about available litters.

I screened the descriptions of parents: I discarded those who weighed more than 70 lbs, as managing Jack in his dotage had been hard on my back. I discarded those who were described as “protective” or “taking some time to warm up to people.” I checked that the parents had passed the relevant genetic tests (for this breed, tests for several eye diseases and hip dysplasia). Then I looked at the remaining breeders’ websites.

The breeders I liked talked about how they raised the puppies: giving them lots of positive experiences. They talked about what they did with the puppies’ parents - agility, nosework, herding. They often had long applications for potential owners to fill out, which asked all the questions they should: How will you exercise this dog? Do you have a fenced yard? What will you do if he is destructive?

I found a litter in Virginia with a male who sounded perfect: confident, social, and by the way athletic. My husband and I stuffed Jenny into the car and drove 9.5 hours to pick up our boy. He cost, by the way, probably more than twice what a rescue puppy would have cost, but I have paid for knowing that he is clear of some genetic diseases for which he might have been at risk, and for knowing that he was in the uterus of a calm, happy mother; raised with a litter who had plenty of high quality food and safe places; and had extensive early socialization (including the Early Neurological Stimulation and Early Scent Stimulation programs). He has proven, in his first week and a half with us, to be social and sweet, willing to settle down when asked so long as he is given plenty of exercise and mental stimulation, and terrifyingly smart. He and Jenny are already wrestling for hours daily, laying the foundation for what I trust will be a long friendship.

That is the story of how we found Dashiell.

Dashiell

Corrigendum on a recent tame fox article

I came across a new article on the Russian tame foxes today, Russian geneticist repeats dog domestication with foxes in just fifty years. It's a nice summary of the Farm Fox Experiment, although I’m not sure why I've seen two stories covering the tame foxes this week — there’s nothing new going on with them! Why two stories in such a short time period?
 

This article does have a few mistakes in it:

 

[Belyaev] and his intern, Lyudmila Trut, wandered around Russia searching for foxes to start their experiment. Foxes were chosen based on their behavior in the presence of humans. Those that showed slightly more tolerance of humans were brought back to their Novosibirsk lab to serve as the start group.

and his intern, Lyudmila Trut, wandered around Russia searching for foxes to start their experiment. Foxes were chosen based on their behavior in the presence of humans. Those that showed slightly more tolerance of humans were brought back to their Novosibirsk lab to serve as the start group.

Read more at: http://phys.org/news/2016-09-russian-geneticist-dog-domestication-foxes.html#jCp

and his intern, Lyudmila Trut, wandered around Russia searching for foxes to start their experiment. Foxes were chosen based on their behavior in the presence of humans. Those that showed slightly more tolerance of humans were brought back to their Novosibirsk lab to serve as the start group.

Read more at: http://phys.org/news/2016-09-russian-geneticist-dog-domestication-foxes.html#j

and his intern, Lyudmila Trut, wandered around Russia searching for foxes to start their experiment. Foxes were chosen based on their behavior in the presence of humans. Those that showed slightly more tolerance of humans were brought back to their Novosibirsk lab to serve as the start group.

Read more at: http://phys.org/news/2016-09-russian-geneticist-dog-domestication-foxes.html#jCp

 

 The original foxes were imported from Canadian fox farms, not chosen from around Russia as this article says. Also, the very first foxes selected for the founding population of the study were not chosen based on their behavior. A control group was kept, so the researchers (of which there are more than two) didn’t want that first set to be more friendly than the average farm fox.

 

[The changes were] not all on the outside—their adrenal glands became more active, resulting in higher levels of serotonin in their brains, which is known to mute aggressive behavior.

 

The tame foxes’ adrenal glands became less active, and secreted less cortisol, a hormone which is associated with stress. Additionally, they have been shown to have higher levels of serotonin in their brains (not secreted by their adrenals, however), which is associated with less aggressive behavior, though I think saying that serotonin “mutes” aggressive behavior might be going a bit far. We don’t fully understand the link between serotonin and aggression.

I do like seeing the Farm Fox Experiment covered in the popular press, though. It’s such a great way of explaining how selection works and such a fascinating demonstration of how quickly selection can have an effect!

And it was not all on the outside—their adrenal glands became more active, resulting in higher levels of serotonin in their brains, which is known to mute aggressive behavior.

Read more at: http://phys.org/news/2016-09-russian-geneticist-dog-domestication-foxes.html#jCpMore importantly, the adrenals don’t control serotonin levels in the brain. They release cortisol into the blood stream. Tame foxes show reduced levels of both cortisol and serotonin compared to control foxes, but those are two different things.

 

Where did dogs come from?

What we know and what we don’t know about dog domestication

Want to learn more about dog domestication? It's not too late to sign up for my online class, From Domestication to Inbreeding!

Dogs evolved from wolves. We’ve been certain of that for several decades by now. But there remain a lot of questions: exactly when did dogs first appear? Did they join their fate with humans when we were hunter-gatherers, or were they attracted to us after the Agricultural Revolution, because we had begun to farm? Which group of ancient wolves did they come from? Knowing more about where dogs began will help us understand modern dogs and their behavior better. Academics are currently conducting a very polite debate about these questions in journals, waged over the course of years.

Grey Wolf

Why is the problem such a hard one? Until recently, the tools that we were using to get information about ancient canids were very limited. Our first tool was archaeology: digging up the remains of ancient canids, trying to figure out if the animal was more dog-like or more wolf-like, and then estimating the age of the find. It’s not entirely straightforward to tell an ancient dog from an ancient wolf using only bones, especially when many archaeological finds are incomplete. The important parts of the skeleton for this work are the teeth and skull: dog muzzles are shorter than wolf muzzles, so that their teeth are more crowded into the available space, and the last premolar and first molar are smaller in dogs than in wolves. Some interesting finds have suggested that dog-like canids first appeared between 15,000-30,0000 years ago — that’s just before agriculture was first developed.

A well publicized 1997 paper from Vilà et al. popularized a new tool for dating dog domestication: analysis of mitochondrial DNA, or mtDNA. Mitochondrial DNA is the DNA inside the mitochochondria in our cells. Mitochondria used to be free-living organisms; they began to live symbiotically in the cells of multi-cellular organisms billions of years ago, but still have their own separate DNA. Mitochondrial DNA gains new mutations at a regular rate, and this can be used as a molecular clock: compare the mtDNA of two different species, and by counting the differences, you can estimate how many years ago the ancestral species split into the two new species.

The problem is that this molecular clock isn’t very reliable or very precise: we don’t really know exactly how fast mtDNA mutates, which makes the clock hard to calibrate. The 1997 findings suggested that dogs and wolves separated about 130,000 years ago — an order of magnitude more than the archaeological estimates suggested! Other mtDNA studies have been conducted since then, with a variety of results, none of them conclusive. It turns out that dog and wolf mtDNA divergence is particularly difficult to analyze because dogs and wolves can and do still interbreed. My golden retriever may not have a wolf in his immediate ancestry, but I suspect you don’t have to go back all that many thousands of years to find one — certainly not all the way back to the domestication split. And there are quite a few populations of dogs in the world with much more recent wolf ancestry than that. This interbreeding really screws up the molecular clock.

In the last few years, though, the revolution in genomic tools — cheap and efficient sequencing of complete genomes — has gotten to the point where it’s affordable to completely sequence the genomes of a number of dogs and wolves for a study. This is significantly changing the kinds of things we can learn about how dogs and wolves genetically differ. Instead of guessing at changes in mtDNA, we can look at the actual genes that differ between the two species. These new studies have set the date of dog domestication at 11,000-32,000 years ago, a date which is similar enough to the archaeological findings to make a lot of sense.

We’ve learned a lot of interesting things from these new sequencing studies beyond just a more precise date of domestication. A little more than a year ago, Axelsson et al. found that dogs make more of an enzyme for digesting starch than wolves do. The enzyme is called amylase, and dogs have multiple copies of the gene, whereas wolves have only one. These researchers wondered if this improved ability to digest starch meant that dogs were domesticated after the appearance of agriculture — if starch digestion was part of the domestication process. However, a study published in January 2014 by Freedman et al. dug deeper into the amylase question and discovered that in fact, not all dogs have extra amylase genes. Some ancient breeds, like the husky, do not. Neither does the dingo. These very recent findings suggest that dogs were in fact domesticated before the Agricultural Revolution, and that some breeds later developed an improved ability to eat what we eat, adapting to their new post-domestication diet. You might imagine that such a change would have been less important to the husky, living in the cold north as it did, where meat was on offer much more often than plants.

Freedman et al. also suggested that dogs didn’t actually evolve from wolves. Wait, what? It's possible that both dogs and wolves evolved from a different ancient canid which doesn’t exist any more. Freedman came to this conclusion using a somewhat complicated genomic analysis which doesn’t tell us anything about what such a canid would have been like, but it’s an idea which resonates with reservations I’ve always had about the “dogs came from wolves” theory. Wolves are so shy, so hesitant to come near humans, and so focused on making their living by hunting. The ancestors of dogs seem more likely to have been scavengers, willing to live close to humans. Maybe some ancient canid did give rise to both species — the one moving closer to human civilization and becoming dogs, the other farther away and becoming wolves. With several studies coming out every year about dog domestication, we may learn more very soon.

For more information, check out “How Much Is That in Dog Years? The Adventof Canine Population Genomics,”a recent open-access review article that provided much of the information in this story.

Note: this story was originally published in the summer 2014 issue of  The APDT Chronicle of the Dog.

Image by Isster17 (Own work) [CC BY-SA 4.0 (http://creativecommons.org/licenses/by-sa/4.0)], via Wikimedia Commons

References

Axelsson, Erik, et al. “The genomic signature of dog domestication reveals adaptation to a starch-rich diet.” Nature 495.7441 (2013): 360-364.

Freedman, Adam H., et al. “Genome sequencing highlights the dynamic early history of dogs.” PLoS genetics 10.1 (2014): e1004016.

Larson, Greger, and Daniel G. Bradley. “How Much Is That in Dog Years? The Advent of Canine Population Genomics.” PLoS genetics 10.1 (2014): e1004093.

Vilà, Carles, et al. “Multiple and ancient origins of the domestic dog.” Science 276.5319 (1997): 1687-1689.