A 50-year experiment on fox domestication was conducted in Novosibirsk, Russia beginning in 1959. The experiment aimed to study the genetic changes underlying animal domestication by selectively breeding foxes for tameness towards humans. Over generations, the foxes selected for friendliness developed morphological traits like floppy ears, curled tails, and spotted coats similar to dogs. The results supported the hypothesis that selection for a single regulatory trait like behavior can induce changes across the genome by destabilizing developmental processes. This provided insights into the genetic mechanisms and parallel changes seen during animal domestication.

1. Domestication as a Model of Speciation 50 years long experiment, run in the Institute of Cytology and Genetics Biology. Summer School 2007 Novosibirsk Marina Voloshina Phys-Math School, Novosibirsk State University, 2007 http://www.slideshare.net/outdoors

2. This is an educational lecture for students – an overview of an experiment conducted by scientists of Novosibirsk Institute of Cytology and Genetics and its evolutionary implications

3. Evolution – changes in genetic programs What kind of changes leads to speciation? Our subject today: The genetic background of evolution

4. Domestication of animals is a long-scale process, which began in prehistoric times Pet or tool? Man walks a dog many thousands years ago http://www.kamat.com/kalranga/rockpain/betaka.htm Rock Painting, Madhya Pradesh, India ~ 12 000 years old

5. Our assistants

6. And pets

7. Domestication is a result of artificial selection , which, opposite to natural selection , is carried out by man. Actually, there is no real opposition between these two kinds of selection – even Charles Darwin began his classical work with amazing examples of variation in domestic animals, caused by man .

8. Darwin’s example of artificial selection – pigeons breeds

9. Darwin considered the man’s job on changing animal’s phenotype and behavior as a model of what nature can do. And as any model it can help us to understand the mechanisms of evolution – the basic process of life history. The problem is that prehistoric people had not bothered of making detailed scientific records for us.

10. In 1959 a group of Siberian scientists, headed by academician Dmitry K. Belyaev , the Director of the Institute of Cytology and Genetics in Novosibirsk, started a large-scale experiment on fox domestication. It lasts ~ 50 years by now

11. Institute of Cytology and Genetics, Novosibirsk, Academgorodok

12. Academician Dmitry Belyaev 1917 - 1985

14. Belyaev’s collaborator. Guides this experiment now Dr. Ludmila Trut

15. It means: The individuals differ by fitness – the most adopted have more chances to survive and to produce offspring hence – to pass their genes to future generations The basic mechanism of evolution is natural selection Charles Darwin

16. Depending on particular phenotypes it favors, the natural selection has several types .

17. The universality of these three patterns is based on some assumptions : The object for selection is some phenotypic trait All traits are equal for selection – any of them can fall under selection pressure and change in similar way The phenotype variation, which is a raw material for selection, is just a manifestation of pre-existing genetic variation , produced by mutation process

18. The real evolution is more complicated. Selection never affect one character only. Because an organism is by no way a mechanical combination of traits, but a highly integrative system The proteins and cells interact in the ontogenesis (individual development) This process has hierarchy – some genes and gene complexes (the master genes ) rule and control other genes activity.

19. The highest integrative levels in animals are nerve and hormonal regulation From this point of view traits become not equal Even slight changes in the regulatory genes can give rise to a wide network of changes in the developmental processes they govern.

20. In highly integrative systems even small changes of one element can lead to an avalanche-like events

21. Regulatory systems The systems make an organism develop and function as a whole Genes , controlling development Hormones Nerve system The hormonal and nerve systems are also defined by genes!

22. Regulatory genes

23. Thus, selecting animals for behavior – the top regulatory character, involving many genes - may lead to other, far-reaching changes in the animals’ development It can cause destabilization of ontogenesis , and by that means changing of many other characters , which had not undergone direct selection

24. The mystery of parallelism These was in line with one of well-known and mysterious facts about domestication: a striking parallelism in the morphological changes In a wide range of mammals – herbivores and predators, large and small – domestication seems to lead to strictly coincident forms

25. all except sheep changes in reproductive cycle dogs, cats, pigs, sheep, goats, cattle floppy ears dogs, cats, sheep shortened tails, fewer vertebrae dogs, pigs rolled tails sheep, poodles, donkeys, horses, pigs, goats, mice, guinea pigs wavy or curly hair all piebald coat color all appearance of dwarf and giant forms Domesticated species Character

26. Can all these modifications be a consequence of a change in one character – behavior ? That was the idea of academician Belyaev, when he started the domestication experiment in 1959.

27. The fox domestication experiment As experimental model was chosen a species taxonomically close to the dog, but never before domesticated: Vulpes vulpes , the silver fox

28. Belyaev began with 30 male and 100 female foxes, most of them from a commercial farm in Estonia Foxes had been farmed since the beginning of XX-th century. The founding foxes were already tamer than their wild relatives The only criterion for selection was tameness – friendly behavior towards human beings

29. Selection was strict : not more than 4 or 5 percent of male offspring and about 20 percent of female offspring have been allowed to breed To ensure that their behavior is determined rather by genes , than by the environment, any training was excluded : the foxes spent their lives in cages and were allowed only brief contacts with humans

30. By behavior tests foxes were divided to 3 classes: Class I – tame . Friendly toward experimenters, wagging their tails and whining

31. Let themselves be petted and handled but show no emotionally friendly response Class II – neutral

32. Class III – wild. Aggressive behavior

33. wild

34. To the 10 th generation of selection 18 % of foxes became elite (best of the Class I). Now days the elite foxes make about 80 %.

36. What distinguishes the domesticated foxes of the wild ones? The first is the behavior Behavior is strictly determined by hormones – and hormone level changed significantly too The reproductive cycle regulated by hormones is very conservative in wild animals. Domestication shifted time of the normal breeding season and even made some animals capable for twice a year reproduc tion . (normally once)

37. 4. More surprising were the morphological changes The new morphological characters that are absent in wild animals but are quite common in dogs: a loss of pigment in the coat color – “Star” mark on the forehead and piebald coat floppy ears rolled tails shortened tails and legs

38. ‘ Star’ heterozygous ‘ Star’ homozygous

40. Domesticated American mink

41. Floppy ears

42. Floppy ears in cats – Scottish-fold

43. Tails curled upwards

44. Shortened tail and legs

45. Questions and answers Why the changes involved so many traits whereas animals were selected for behavior only ? Why the changes are so similar in animals of various systematic groups, domesticated by different people at different times in different parts of the world?

46. Nikolay Vavilov in 1930-th explained the phenomenon of homologous variability (parallelism) by gene homology in species of one lineage Similar genes produce similar mutations Similar mutant phenotype

47. But the frequency of aberrant phenotypes in the population selected for behavior is 10 -2 - 10 - 3 . which is 2 or 3 orders higher than the average frequency of spontaneous mutations This contradicts to mutational explanation of all observed aberrations I n some foxe s several different aberrations appear ed simultaneously – which is statistically imp ossib le if mutations at structural loci are the cause of these change s

48. The answer of Belyaev was that the key is the selection for behavior . He considered the genetic transformations of behavior to be the main factor entraining other genetic events. Many of the genes determining behavior may be regulator y , engaged in stabilizing an organism’s early development, or ontogenesis . Ontogenesi s is an extremely delicate process. In principle, even slight shifts in the sequence of events could throw it into chaos. Thus the genes that orchestrate those events and keep them on track have a powerful role to play.

49. The leading role among genes stabilizing an organism’s development belongs to the genes that control the neural and endocrine systems The same genes govern the systems that control an animal’s behavior, including its friendliness or hostility toward human beings. So, selecting animals for behavior can fundamentally alter the development of an organism.

50. Gene networks rule the development of all traits in ontogeneses Master genes in inductor cells Membrane receprors’ genes Regulatory genes Srtucrural proteins’ genes

51. Most of the novel traits and other changes in the foxes seem to result from shifts in the rates of ontogenetic processes in other words, from changes in the timepoint of genes action Floppy ears, for example, are characteristic of newborn fox pups but become get carried over to adulthood

52. The disintegration of regulatory mechanisms can give chance to manifest to the “sleeping” mutations , which are normally blocked by these mechanisms Recessive mutations can express like dominant in the new hormonal state It leads to the growth of variability of all characters – psychic and morphological.

53. Belyaev’s Idea of Destabilizing Selection Destabilizing Selection is a strong directional selection by an integrative character , that controls ontogenesis. This type of selection provides wide genetic variation by destroying the masking regulatory mechanisms .

54. The idea explains the parallelism in evolutionary changes of domesticated animals of different taxonomic groups. Indeed, if the regulatory mechanisms – nerve and hormonal – are similar in all Mammals, then destabilizing of them would lead to similar phenotypic changes. Belyaev’s Idea of Destabilizing Selection

55. Destabilizing Selection as a Model of Speciation A puzzle of speciation is that species seem to be stable for a long periods of time And then suddenly (in geological time scale) disappear (in case of extinction) or transform to a new species. Thus, speciation is relatively fast process (hundreds - thousands generations) in comparison with species continuance.

56. Stasis, Extinction and Speciation

57. Species stability is maintained by stabilizing selection Ivan Shmalgauzen 1884 - 1963 It provides genetic homeostasis . All genes act in coordinate way, resulting in normal development

58. But stabilizing selection is effective in stable environment only If environment abruptly changes – the average fitness of population falls dramatically and directional selection for previously rare phenotypes began

59. These extreme phenotypes may be not balanced with other genes – because synchronizing gene orchestra takes time. The population enters the period of instability. new equilibrium. extinction.

60. This model of speciation was put forward by Stephen Jay Gould in 1970-th

61. Punctuated Equilibrium Theory of Speciation

62. This theory strongly resembles processes observed in domestication Of course, natural selection, leading to speciation should not always affect behavior Selection may act on any regulatory chain

63. For example, strict change of environment can provoke stress – intensive emotional pressure. Stress leads to long-time hormonal changes and selection for stress-resistance genes – regulatory kind of genes, like genes of behavior

64. The recent results from molecular study of genomes come in line with this view on speciation They revealed that most of general changes in organism’s structure are result of changes in gene regulation , their spatial and temporal pattern of expression , rather than direct changes in their DNA sequence

65. Regulatory evolution at the yellow gene underlies the wing pigmenation of Drosophilidae Staining for yellow protein D.melanogaster D. biarmipes D. guttifera Wings

66. Domestic Animals: Parallelism in Color

69. Humans and dogs – convergent evolution? http://email.eva.mpg.de/~tomas/pdf/Hare_Tomasello05.pdf

70. Implications of Domestication Mechanisms for H uman C ognitive E volution This recent comparative work suggests that human-like social intelligence could initially have evolved, not as an adaptation, but rather as a by-product of selection on social-emotional systems – perhaps supported primarily by limbic and endocrine systems rather than the neocortex

71. Links Wikipedia article http ://en.wikipedia.org/wiki/Tame_Silver_Fox Lyudmila Trut. Early Canid Domestication: The Farm-Fox Experiment http://www.americanscientist.org/my_amsci/restricted.aspx?act=pdf&id=3038739723681 Website of the Cornell University on the collaboration work with the Institute of Cytology and Genetics, Novosibirsk http ://cbsu.tc.cornell.edu/ccgr/behaviour/Index.htm What Can Dogs And Silver Foxes Tell Us About Each Other? http ://cbsu.tc.cornell.edu/ccgr/behaviour/04_Recent_Publications/FoxChapter.pdf B.Hare and Michael Tomasello. Human-like social scills in dogs? http://email.eva.mpg.de/~tomas/pdf/Hare_Tomasello05.pdf

72. Copyright notice This is an educational presentation, based on works of D.K. Belyaev and L.N.Trut of the Institute of Cytology and Genetics. You can use it in education with the links to original works. Any commercial use is prohibited. You have no right to place it on any website or portal for download. Marina Voloshina http :// www.slideshare.net / outdoors http:// biologii.net