1. The Cognitive Dog Class 2: The Great Debate Bruce Blumberg & Carolyn Barney Harvard Extension School

2. Agenda for class Questions from last week Plan for next week Some warm-up questions The great debate

3. Plan for next week The behavior of wolves and wild canids Readings Jensen, Chapters 7 & 9. Optional: Packard, J. M. (2003). Wolf Behavior: Reproductive, Social and Intelligent. Wolves:Behavior, Ecology and Conservation.

4. Warm-up Questions... What is the difference between Domesticated and Tame? What characteristics do domesticated species share? Why are there only 100 domesticated species, more or less, out of roughly 50,000 species of vertebrates? Out of the 100 domesticated species, how many, do you think, are used in competitions that require some level of training by humans? What characteristics, do you think, makes a species “easy to train?”

5. More Warm-up Questions... What do you think Udell was getting at by the title of her paper? What was the big idea of the Horowitz paper? Even a few second (e.g, 2 sec. vs. 4 sec) delay of reinforcement/punishment has dramatic effect on its effectiveness (Azzi, Camp...). Why do you think this is? How might this contribute to the Horowitz result?

6. Even More Warm-up Questions... What is a MAP? What is a Key Releaser? What does it mean for something to be innate? How can you tell if something is innate?

7. Domestication “that process by which a population of animals becomes adapted to man and to the captive environment by genetic changes occurring over generations and environmentally-induced developmental events reoccurring during each generation” * How... Artificial Selection Natural Selection Relaxation of Natural Selection Differential expression of genes pre-existing in population What is the exact nature of the genetic change and the interplay between genetic changes and environmentally-induced developmental events? * Price, E. O. (1998). Behavioral Genetics and the Process of Animal Domestication. Genetics and the Behavior of Domestic Animals. T. Grandin. San Diego, Academic Press: 31-65.

8. In fact there are 4 big questions to ask... Causation: what elicits the behavior, and are there learned components? Function: how does it enhance survival? Development: when does the behavior appear and what role does development & developmental context play? Evolution: do you see it in related species how might it have arisen via evolution? Niko Tinbergen

9. The debate: the evolution of human-like social skills in dogs?

10. A word to the wise “we agree with one of our reviewers saying that the present state of this field does not allow for scientific arguments on social cognition evolution” - Adam Miklosi & Krisztina Soproni Miklosi, A. and K. Soproni (2006). "A comparative understanding of the human pointing gesture." Animal Cognition 9: 81-93.

11. Miklosi, A., J. Topal, et al. (2004). "Comparative social cognition: what can dogs teach us?" Animal Behaviour 67(6): 995. Really about the evolution of social cognition Hungry UK A bit of a cottage industry

12. Pointing gestures as cues Experiments do try to control for olfactory cues Hare, B. and M. Tomasello (2005). "Human-like social skills in dogs?" Trends in Cognitive Science 9(9): 339-444 Miklosi, A. and K. Soproni (2006). "A comparative understanding of the human pointing gesture." Animal Cognition 9: 81-93.

13. Attentional state as cues Is the dog more likely to grab the treat if the person isn’t facing them? Call, J., J. Brauer, et al. (2003). "Domestic Dogs (Canis Familiaris) Are Sensitive to the Attentional State of Humans." Journal of Comparative Psychology 117(3): 257-263.

14. Attentional state as cues Is the dog sensitive to the apparent attention of the person? Viranyi, Z., J. Topal, et al. (2004). "Dogs respond appropriately to cues of humans' attentional focus." Behavioural Processes 66(2): 161.

15. Words as labels What is the mechanism behind word use?

16. Experiments generally show that dog’s choice is biased by gestural cues These results are more or less typical Miklosi, A., P. Pongracz, et al. (2005). "A Comparative Study of the Use of Visual Communicative Signals in Interactions Between Dogs (Canis Familiaris) and Humans and Cats (Felis catus) and Humans." Journal of Comparative Psychology 119(2): 179-186.

17. Using dogs as a model to understand the evolution of social cognition in humans Why the the funding agencies care Hare, B. and M. Tomasello (2005). "Human-like Social Skills in Dogs." Trends in Cognitive Science 9(9): 439-447.

18. Another word to the wise Scientific work almost always needs to be seen through the lens of the intellectual, social and funding context in which this work was done

19. Why? Evolution of social cognition in humans is a “hot” topic The argument is that dogs represent a really interesting animal model Highly social Presumably their behavior has been selected for success in the ecological niche of human-dog social groups. Dogs “are enculturated” vs. Chimps who “can be enculturated” Easy to find experimental subjects Everybody likes a good dog story

20. Why I/we care... What can we learn that will help us understand why the dogs in our households do what they do how to better raise behavorally-healthy dogs how to better train and interact with our dogs how to better ensure that our dogs stay behaviorally healthy.

21. Hare 2002 - 2005

22. Hare 2002 The difference between dogs & chimps was startling, and the question was why? Hare, B., M. Brown, et al. (2002). "The domestication of social cognition in dogs." Science 298: 1634-1636. 9 out of 11 dogs used cue vs. 2 out of 11 for chimps

23. Hare’s Three Hypotheses (2002) “Canids in general are unusually flexible in the types of social information they can exploit” “Domestic dogs... have learned their skills during their individual ontogenies” “Selection pressure on dogs during process of domestication for specific skills of social cognition and communication with humans”

24. Dogs performed differently than ‘socialized’ wolves This suggested to Hare that it wasn’t an ability common to canids Hare, B., M. Brown, et al. (2002). "The domestication of social cognition in dogs." Science 298: 1634-1636. No wolf performed above chance using any cue. 7 dogs used GPT, 5 used GP, 4 used P to find food above chance. 3 dogs used all 3 cues, 3 dogs used 2, and 1 dog used just one. Gaze, point, touch Gaze, point PointControl

25. Litter raised pups did the same as family raised pups This suggested to Hare that it wasn’t developmental Hare, B., M. Brown, et al. (2002). "The domestication of social cognition in dogs." Science 298: 1634-1636. Differences aren’t significant, but interesting that litter-reared did better than family raised.

26. 9-12 week pups did as well as 17-24 week pups This suggested to Hare that there wasn’t a learned component

27. Hare’s big conclusion “These findings suggest that during the process of domestication, dogs have been selected for a set of social-cognitive abilities that enable them to communicate with humans in unique ways.”

28. Things to think about... Are there flaws with the experimental design and analysis? There is an assumption that socialized wolves are the same as socialized dogs. Is this valid? There is an assumption that extensive contact with humans prior to 8-12 weeks is required for pups to preferentially attend to humans. Is this valid? There is an assumption that social learning doesn’t occur prior to 8-12 weeks. Is this valid? There is an assumption that you can describe a generic pet dog, and that one can generalize across breeds. Is this valid?

29. Things to note about experiments Small number of subjects with repeated trials Criteria is statistically different than chance Results are typically aggregated Typically subjects are adult pet dogs recruited from local training clubs, friends, etc. Class 11 we will revisit methodology because it is often problematic

30. Hare 2005 Hare’s statement: “dogs have an unusual ability for reading human communicative gestures... seems to have evolved during domestication” Hare’s question: “unclear whether this evolution occurred as a result of direct selection for this ability... or as a correlated by-product of selection against fear and aggression toward humans” Decided to test hypothesis using domesticated foxes that were explicitly bred to have reduced fear and aggression toward humans Hare, B., I. Plyusnina, et al. (2005). "Social Cognitive Evolution in Captive Foxes Is a Correlated By- Product of Experimental Domestication." Current Biology 15: 226-230.

31. Belyaev’s foxes... Trut, L. (1999). Early Canid Domestication: The Farm Fox Experiment. American Scientist. 87: 160-169 we will keep coming back to Dr. Belyaev & his foxes

32. Belyaev’s Fox experiment... Criteria for breeding Flee threshold Flee distance later generations, willing to approach After 18 generations they had produced foxes that had some ‘dog-like’ behavioral and morphological characteristics...

33. Pups & domesticated fox kits performed similarly This suggested to Hare that this skill was a by product of selection for tameness Hare, B., I. Plyusnina, et al. (2005). "Social Cognitive Evolution in Captive Foxes Is a Correlated By- Product of Experimental Domestication." Current Biology 15: 226-230. Pups & fox kits between 8-16 weeks

34. Temperament of farm foxes may interfere with performance This experiment was consistent with Hare’s view that this skill was a side-effect of breeding for temperament Hare, B., I. Plyusnina, et al. (2005). "Social Cognitive Evolution in Captive Foxes Is a Correlated By-Product of Experimental Domestication." Current Biology 15: 226-230.

35. Hare’s conclusions... 2 alternative explanations for dog’s ability to read human signals Communication hypothesis: this ability was directly selected for during domestication Correlated by product hypothesis: this ability is simply a by-product of selection for tameness He believes his results support correlated by-product hypothesis... Nothing was being selected for other than tameness (e.g., ability to read human cues) and yet foxes did as well as pet dog pups

36. Things to think about... At one level, all Hare is saying is that cognition takes place in an emotional context. This highlights the central role that emotions and temperament play in a dog’s choice of what to attend to, and what to do. This is why we devote so much time to emotion and temperament What are the specific mechanisms that make a pet dog emotionally prepared to interact & attend to humans? Can we tease apart the complex interplay of genes, development, developmental context, & learning? This is why we devote so much time to development

37. Is this the whole story? Hare’s argument: lowered emotional reactivity was selected for, and at a minimum, this set the stage. How much more is needed? Miklosi’s argument: that is not the whole story, social skills were selected for as well...

38. Kubinyi et al, 2007

39. Social evolution: from wolf and dogs to humans Research question: can we use the presumed evolution of social cognition in dogs to say anything about the evolution of social cognition in humans? They claim dogs are an interesting model because... “Behavior changed in a way that made them successful in the human social environment” “Behavior of dogs’ ancestor species can be reconstructed from the behavior of the wolf” “The natural socialization of dogs in the human environment offers a parallel between them and children. Kubinyi, E., Z. Viranyi, et al. (2007). "Comparative Social Cognition: From wolf and dog to humans." Comparative Cognition & Behavior Reviews 2: 26-46.

40. Unique evolutionary history... Dogs were first domesticated animals (when this occurred will be a topic for another lecture...) Their model subset of wolves adapted to new ecological niche provided by humans traits implicitly/explicitly selected for by humans Explicit selection for behavioral and morphological traits (19th century) produced dog breeds.

41. The family wolf project: if wolves are raised like pet dogs, do they act like pet dogs? They take as a given that dogs and wolves have a very different developmental time course... Critical period for socialization seems to begin prior to 10 days in wolves vs. 3 to 5 weeks in dogs, and in dogs it extends up to 12 weeks. In wolves, 24/7 contact with humans seems to be required In pet dogs, minimal contact/presence seems to be enough to scaffold social attraction to another species (such as humans...) Presence/absence of litter-mates seems to have a different effect in wolves vs. dogs. Why this should be is the most fascinating question of all to me!!!!!!!!

42. Its a tough job but somebody has to do it :-) 13 wolf cubs & 11 pups Raised similarly Tracked comparative behavior over approximately 2 years “... intensive early handling proved to be an effective means of socializing wolves to a level comparable to dogs...” The family wolf project Kubinyi, E., Z. Viranyi, et al. (2007). "Comparative Social Cognition: From wolf and dog to humans." Comparative Cognition & Behavior Reviews 2: 26-46.

43. Statistically different performance on attachment test... Must depend on more than social experience... Kubinyi, E., Z. Viranyi, et al. (2007). "Comparative Social Cognition: From wolf and dog to humans." Comparative Cognition & Behavior Reviews 2: 26-46.

44. Pet dogs seem to be able to use pointing gestures more easily... “dog puppies as young as 4 months old are able to perform well... without any special, intensive, and early socialization to humans” Significant difference in performance between 4 month old wolf cubs and pet dog pups, but... “After extensive training, wolves significantly improved in parallel with increased readiness to look at the pointing human.” Kubinyi, E., Z. Viranyi, et al. (2007). "Comparative Social Cognition: From wolf and dog to humans." Comparative Cognition & Behavior Reviews 2: 26-46.

45. Wolves may be less likely to look at people Tested wolves are significantly less likely to look to their handler when working on a blocked task, and when they do look, spend less time looking. Attention is a prerequisite for learning. If wolves are biased against, or dogs biased toward attending to humans one would expect a difference in... Learning to use human generated cues Use of those cues to guide behavior Kubinyi, E., Z. Viranyi, et al. (2007). "Comparative Social Cognition: From wolf and dog to humans." Comparative Cognition & Behavior Reviews 2: 26-46.

46. Miklosi’s interpretation Wolves aren’t as good at using human cues as dogs because of “their decreased willingness to look at the human” Conversely, “preferential looking at the human seems to be a genetic predisposition of dogs”... at this is the “foundation on which developmentally canalized complex communicative interactions can emerge between man and dog” In other words, a genetic bias to look at people was a precursor to the coevolution of dog-human communicative skills. Miklosi, A., E. Kubinyi, et al. (2003). "A Simple Reason for a Big Difference: Wolves Do Not Look Back at Humans, but Dogs Do." Current Biology 13(9): 763.

47. Miklosi et al call this apparent difference in attention: “A simple reason for a big difference” They suggest 2 processes might have been at work... A bias to attend to people, and all that that brought along with it, may have been implicitly or explicitly selected for Natural or artificial selection Lower emotional reactivity in dogs may allow dogs to “tolerate being gazed at by humans better than wolves” In either case: a genetic bias to look at people may have been a precursor to the co- evolution of dog-human communicative skills.

48. Some things to keep in mind... Any bias that exists in dogs... may be to members of an imprinted species rather than limited to humans (e.g., live stock guarding dogs raised with sheep). may have a wide variance across individual dogs and across breeds, e.g. a border terrier trying to get a rat in a cage doesn’t spend a lot of time looking back at its handler either... it may well have arisen as a side-effect of some other difference... There doesn’t need to be, and mostly likely isn’t, a gaze-at-human gene. May not have been directly selected for.

49. In the end... The course will focus on many of the issues that are at the heart of much of the work described above. origins of the dog development emotion & temperament social learning

50. Next week: wolves & wild canids