The Cognitive Dog

1. The Cognitive Dog • Class 7: Evolution and Development

2. A couple of quick things... • Problem set due 4/12 • Next week: Jensen chapters 10 & 11, Serpell • Nature Article on origins of dog. NYT summary: http://www.nytimes.com/2010/03/18/science/18dogs.html?emc=eta1 • Coppinger & Lord talks

3. Artificial selection for temperament produced some unexpected side-effects...

4. Trut, L. (1999). Early Canid Domestication: The Farm Fox Experiment. American Scientist. 87: 160-169 Belyaev’s foxes... • Dr. Belyaev & his foxes

5. Trut, L. (1999). Early Canid Domestication: The Farm Fox Experiment. American Scientist. 87: 160-169 Q: does selection for behavior have unexpected side effects?

6. “Star”: seeing vs. looking... • Great advances often come from seeing things others overlook or deem uninteresting, and asking how come? • It is worth noting that he did find what he set out to look for... • This can introduce bias... Trut, L. (1999). Early Canid Domestication: The Farm Fox Experiment. American Scientist. 87: 160-169

7. Belyaev’s Fox experiment... • Started with a population of 465 foxes • 30% extremely reactive • 40% moderately reactive • 20% fearful • 10% quiet & exploratory

8. Belyaev’s Fox experiment... • Criteria for breeding • Flee threshold • Flee distance • later generations, willing to approach • After 18 generations they had produced foxes many of which had ‘dog-like’ behavioral characteristics and some had similar morphological ones...

9. 45,000 foxes, 40 years and 35-40 generations later... • 70-80% of foxes are ‘domestic elites’ • Morphological changes • shorter but wider skulls, overall smaller skulls especially in males • biannual estrus displayed in 2 lines (no litters however) • floppy ears, curly tails, piebald coats occur, but at a low rate: ‘a few animals per hundred’. • On average, significant changes in patterns of development...

10. Trut, L. (1999). Early Canid Domestication: The Farm Fox Experiment. American Scientist. 87: 160-169 Significant change in timing of developmental milestones • longer and earlier period of socialization

11. Trut, L. (2001). Experimental Studies of Early Canid Domestication. The Genetics of the Dog. A. Ruvinsky and J. Sampson. Wallingford, UK, CABI Publishing: 564. Significant change in timing of developmental milestones • More details...

12. Cortisol levels are different... Stress • Hormone produced by the adrenal gland, especially during stress. Level is an indicator of stress. • Viewed as having an important effect on memory & emotional processes • Levels do not rise as sharply, nor as high in domesticated foxes vs. farm foxes. Dom. foxes more likely to explore. Exploration Exploration Stress Trut, L. (2001). Experimental Studies of Early Canid Domestication. The Genetics of the Dog. A. Ruvinsky and J. Sampson. Wallingford, UK, CABI Publishing: 564.

13. Trut, L. (2001). Experimental Studies of Early Canid Domestication. The Genetics of the Dog. A. Ruvinsky and J. Sampson. Wallingford, UK, CABI Publishing: 564. In utero they are exposed to lower levels of cortisol

14. Trut suggests... • Glucorticoids have a regulatory function during development... • Circulating glucorticoids in uterus have an impact on the timing of cell division and differentiation • “The level of these hormones and the timing of their appearance in in vivo may be involved in the regulation of the duration of developmental processes.” • Many of the neurotransmitters also play a role in regulating the rate of development, so changes in when those systems come on line and their levels could have morphological side-effects. • Tightly coupled with pigment production, selecting for behavior may have side-effect of coat coloration and vice-versa! Trut, L. (2001). Experimental Studies of Early Canid Domestication. The Genetics of the Dog. A. Ruvinsky and J. Sampson. Wallingford, UK, CABI Publishing: 564.

15. Trut... • “Most probably, the ... changes... were caused by changes in a few genes. However, their function(mission) was to integrate entire development as a whole... occupied the highest level in the hierarchical structure of genome expression regulation. Even small changes at this high level of regulators could produce a cascade of changes in gene activity and, as a consequence, rapid and extensive changes in the phenotype.” • The effect of domestication may have been to alter a small number of genes that play a role in regulating development, and even a small change could have had profound side-effects Trut, L. (2001). Experimental Studies of Early Canid Domestication. The Genetics of the Dog. A. Ruvinsky and J. Sampson. Wallingford, UK, CABI Publishing: 564.

16. Coppinger: how the dog may have evolved via natural selection & post zygotic selection...

17. The two contrasting views... • Artificial selection... • “People tamed and trained wild wolves and turned them into dogs” • Natural selection... • “One or more populations of wolves domesticated themselves”

18. Coppinger’s hypothesis • “My hypothesis is that dogs are coincident with permanent human settlement. It is the change in human behavior that creates the niche that wolves exploit and adapt to...”

19. And a mighty good niche it is... • One way or another dogs are by far the most successful canid... • 400,000 wolves • 4,000,000 coyotes • 40,000,000 jackals • 400,000,000 dogs (100X number of wolves)

20. How he presents his argument • Argues that the “pinocchio” hypothesis has critical flaws... • Uses two different arguments to show why his hypothesis could be plausible... • The Belyaev fox experiment • Role of dogs in modern day “Mesolithic/Neolithic” villages

21. Pinnochio hypothesis • Early humans actively tamed, trained and presumably bred ever tamer & more trainable wolves/dog • The problem is that wolves are hard to tame... • Must be taken away from Mom 8-14 days after birth & mothered by human 24/7 (including bottlefeeding) • Wolves have a very pronounced fear period that works against even early socialization

22. Reactivity also casts doubt on Pinnochio • Gross generalizations but... • Wolves are fearful of novelty especially in “home” environment • Level of fear may interfere with the kind of training we do with dogs (remember learning occurs within an emotional context.

23. Speciation requires populations • Coppinger questions exactly how Mesolithic people would have gone about breeding ever-tamer wolves... • sort through natural population • find variations in natural tameness • isolate tamer wolves from rest of population • breed only the most tame ones • repeat...

24. Practical questions... • Feeding tame wolves • Remember from MacDonald that size matters! • Breeding • Breeding in captivity is hard (stress) • Photoperiodic (once a year) • Reality of living on the margin • Exactly how does hunting work with a wolf anyway?

25. So he suggests... • The village as a new niche • Wolves invade niche and gain access to a new food source • Niche favors scavengers not predators (those that can get by on less energy) • Wolves that are genetically predisposed to show less flight distance may be better able to use food source • Don’t run away as soon, run less distance, return quicker, • These tamer wolves gain selective advantage

26. Coppinger in depth... • The human village as a new ecological niche emerged around 15,000 BP • Note: timing is consistent with fossil & genetic timing • Food waste & human waste accessible to animals that can take advantage of it. • Big deal: 70-90% of pups in a pack die of starvation

27. Coppinger in depth... • Natural genetic variation in reactiveness • Those wolves with less reactiveness (to people) • Closer threshold distance before fleeing • Shorter flee distance • Shorter time before returning • Eat in close proximity to people • Result: at food longer, use less energy when they do react.

28. Coppinger in depth • Population sorts out between 2 sub-populations • Less reactive animals that can feed in close proximity to people. Percentage of this sub-population grows. • More reactive animals that can’t use human food sources as effectively. Percentage of this sub-population shrinks

29. Coppinger in depth... • Morphological changes accompany shift in food source from prey to the waste products of human society... • scavengers vs. predators • frequent small meals vs. rare but large meals • big brains and bodies become a liability vs. an asset

30. Darwin’s hypothetical question • How to explain morphological & behavioral changes that distinguish dogs from wolves but whose function is hard to imagine... • Floppy ears and curly tails • Multi-colored coats • Heat twice a year • Barking all the time • Belyaev’s fox experiment suggests a mechanism

31. But Belyaev was all about artificial selection. Doesn’t this just prove... • Belyaev’s experiment demonstrates that selection, be it artificial or natural or some combination, based on “flight threshold, distance and recovery” is sufficient to produce many of the hallmarks of dog behavior and morphology. • The key suggestion of Coppinger is that this selection could have, at a minimum, and in fact, most likely did occur without human intervention.

32. Natural selection vs. artificial selection... • Does it have to be either/or? No, and Coppinger even says as much... • “Two things are happening here with these adaption processes. First, the dogs are evolving more tameable-trainable personalities, and people are facilitating that evolution without ever purposely breeding a single animal. Second, whatever distinguishes the chosen puppy is more likely to appear in the next generation...” • Dogs may have found a niche in which slacking off was the evolutionarily smart thing to do.

33. Just ‘cause its there, doesn’t mean its adaptive Evolved to allow other members of pack to locate dog when running through high prairie grass thus increasing chances dog wouldn’t get separated from pack and lose opportunity to reproduce

34. Part 2: Development

35. Development: growing the shape of the brain • “...while the dog is in its first few weeks of life, and growing its brain, it is making the cell connections and re-arranging them in a specific way, according to the signals that are coming from outside. This development predetermines its adult behavior” - coppinger • “Each behavioral system — fear, submission, investigation, play — has its own rate of development, and varies among breeds. Each is dependent on glandular development and hormone secretions, as well as motor coordination and sensory perception. And each feeds back on the puppy to change not only the shape of the brain...” - coppinger Coppinger, R. and L. Coppinger (2001). Dogs: A Startling New Understanding of Canine Origin, Behavior, and Evolution. New York, NY, Scribner.

36. Growing the shape of the brain... • “Behavior is (always) epigenetic – above the genes – an interaction between the genes and the developmental environment” -Coppinger • Genes play a central role in the timing of developmental events, the rate of development, and duration of developmental periods. Small changes can have huge effects by altering when systems come on line relative to one another. • The resulting behavioral form of the animal emerges from the interaction of the genes and the developmental environment. • Evolution takes advantage of regularities in the developmental environment, e.g., mom, con-specifics, lack of mobility. The evolving genes rely on those regularities.

37. Growing the shape of the brain... • What you see is “the coaction of nature & nurture” • “evolution involves changes in the developmental system (of which the genes are an essential part) but not necessarily changes in the genes themselves... alterations in development may cause genes to become active in the developmental process that were heretofore quiescent...” -Gottlieb • In other words, systematic change in developmental context can produce systematic change in behavioral and/or morphological trajectory, without changing “genes” • Nature and Nurture: each is “on tap” as opposed to “on top Gottlieb, G. (1991). Individual Development and Evolution: The Genesis of Novel Behavior, Oxford University Press.

38. Growing the shape of the brain. • “Behavioral conformation here is a description of the behavioral shape — how the dog moves — when a dog is working” • “Behavioral conformation and physical conformation, in the final analysis, are one and the same.” • “It is not that border collies have genes for herding, but rather, because of gene action, they end up with a differently shaped brain than other breeds” Coppinger, R. and L. Coppinger (2001). Dogs: A Startling New Understanding of Canine Origin, Behavior, and Evolution. New York, NY, Scribner.

39. Critical Periods & Imprinting(love of the familiar)

40. Critical (sensitive) periods • From Scott & Fuller... • “...we mean a special time in life when a small amount of experience will produce a great effect on later behavior” • “The difference between the amount of effort needed to produce the same effect at different periods determines just how critical the period is”

41. Example: gottlieb’s mallards • Experience tunes perceptual mechanism... • Mallards need to hear themselves or sibs vocalize in the shell in order to respond specifically to mom mallard’s call...

42. Example: Song bird learning... • ‘Innate’ coarse template • Sensitive period in which they tune template to dialect of surrounding con-specifics • Months later begin to practice song, matching production to template Bolhuis, J. and L. Giraldeau, Eds. (2005). The Behavior of Animals. London, UK, Blackwell Publishing.

43. Imprinting • Some species have a critical period in which they rapidly establish social bonds in a process called “imprinting” • Filial (mom & my buddies) and sexual • Often different periods for each • Surprisingly flexible (more about being in the right place at the right time)... • Probably tuned to certain features, and then use those to build more complete perceptual model • Probably a type of associative learning

44. Imprinting... • Bruce’s theory... • It is scaffolding that serves to quickly & coarsely identify potential social partners (gets you in the ballpark) • The world of a juvenile animal is such that even the coarsest mechanism may work most of the time... • Effect is to subsequently bias attention toward those partners • Biased attention makes it easier to learn more about characteristics of partners (refine model)

45. S&F on imprinting in dogs • “Whether rewarded, punished, or treated indifferently, the young animal of the proper age proceeds to form an emotional attachment to whatever is present in the environment at that time. The essential mechanism appears to be an internal process acting on the external environment. In this way it is indeed quite different from conditioning, which is directly dependent on outside circumstances” • “To state it more clearly: a young animal automatically becomes attached to individuals and objects to which it comes into contact during the critical period” Scott, J. P. and J. L. Fuller (1965). Genetics and the Social Behavior of the Dog. Chicago, Chicago University Press.

46. Is it all about food? • S&F and company did experiments in which the dogs were... • fed by machines, but presumably handled by people • fed by people, but minimal handling • punished for approaching people (don’t try this at home) • raised in field with minimal handling but daily exposure Scott, J. P. and J. L. Fuller (1965). Genetics and the Social Behavior of the Dog. Chicago, Chicago University Press.

47. Is it all about food? • “might be formed merely by having the person in sight at frequent intervals” • “feeding is not a necessary part of the development of the social bond...[indeed] feeding by itself does not produce a highly socialized animal” • “formed an attachment in spite of considerable punishment. We must remember that these were fox terrier puppies...” Scott, J. P. and J. L. Fuller (1965). Genetics and the Social Behavior of the Dog. Chicago, Chicago University Press.

48. When surrounded by other species dogs will imprint on them too... • Dogs will imprint on • Cats • People • Sheep • ... • Note: dogs can imprint on multiple species simultaneously if in an environment with multiple species...

49. Coppinger: How to grow an LGD vs. a Herding Dog • How to raise a live stock guarding dog... • Raise the pup among sheep for its first 16 weeks... • The effect is that the dog “treats sheep as its primary social companions.” • How to raise a herding dog... • Raise it among people & dogs for the first 4 months... • Introduce it to sheep at 4 months plus... • Sheep do not become primary social companions, people and dogs are

50. Motor Patterns & Critical Periods • An consistent pattern of movement displayed by animals of a species. • Innate (genes + development), sometimes referred to as “prefunctional” • You can observe motor patterns, but you can only infer function. • Examples: eye-stalk, chase, grab-bite, tongue flick...