Влияние экспериментальной доместикации серебристо-черных лисиц (Vulpes vulpes) на вокальное поведение

Статья обобщает цикл исследований структуры звуков и вокального поведения серебристо-черных лисиц, различающихся по характеру реагирования на человека. Показано, что селекция в течение 50 лет на ручное поведение к человеку привела к избирательному использованию Ручными лисицами по отношению к людям двух типов звуков, кудахтанья и шумного дыхания. При этом селекционированные на агрессию к людям Агрессивные и не селекционированные Контрольные лисицы, в свою очередь, избирательно используют по отношению к людям такие звуки, как кашель и фырканье. Таким образом, выявлены типы звуков, являющиеся вокальными индикаторами дружелюбного и агрессивного поведения лисиц по отношению к человеку. Однако доместикация не изменяет вокального поведения лисиц по отношению к другим лисицам, все три группы не различаются по вокальному поведению, адресованному конспецификам. Исследована связь вокального поведения со степенью толерантности по отношению к человеку у гибридов первого поколения от скрещивания между Ручными и Агрессивными лисицами и беккроссов на Ручных и Агрессивных лисиц. Оценен эффект пола лисиц и степени воздействия со стороны человека на параметры вокального поведения. В результате исследований были обнаружены универсальные для млекопитающих вокальные индикаторы степени эмоционального возбуждения, не зависящие от знака эмоций. Выявлены характеристики вокального поведения, связанные со знаком эмоций – позитивным или негативным. Разработан простой и эффективный метод оценки уровня дискомфорта животного на основе «слитых звуков», которые учитывают характеристики всех звуков, изданных животным независимо от структуры этих звуков. Полученные результаты служат основой для дальнейших сравнительных исследований акустической структуры и вокального поведения других представителей рода Vulpes и других близких родов псовых (Canis, Cuon, Lycaon).

1. Beckers G.J.L., Nelson B.S., Suthers R.A. Vocal-tract filtering by lingual articulation in a parrot. Curr. Biol. 2004;14:1592-1597.

2. Belyaev D.K. Destabilizing selection as a factor in domestication. J. Hered. 1979;70:301-308.

3. Belyaev D.K. Destabiliziruyushchiy otbor kak faktor domestikatsii [Destabilizing selection as a factor in domestication]. Genetika i blagosostoyanie chelovechestva [Genetics and Humanity Well-being]. Moscow: Nauka Publ., 1981;53-66. (in Russian)

4. Belyaev D.K. Destabiliziruyushchiy otbor [Destabilizing selection]. Razvitie evolyutsionnoy teorii v SSSR (1917–1970-e gody) [Development of the Evolutionary Theory in the USSR (1917–1970)]. Leningrad: Nauka Publ., 1983;266-277. (in Russian)

5. Belyaev D.K., Trut L.N. Konvergentnyy kharakter formoobrazovaniya i kontseptsiya destabilizirueshchego otbora [Convergent character of shape-creating and the concept of destabilizing selection]. Vavilovskoe nasledie v sovremennoy biologii [Vavilov’s Heredity in Modern Biology]. Moscow: Nauka Publ., 1989;155-189. (in Russian)

6. Berry D.A., Herzel H., Titze I.R, Story B.H. Bifurcations in excised larynx experiments. J. Voice. 1996;10:129-138.

7. Briefer E.F. Vocal expression of emotions in mammals: mechanisms of production and evidence. J. Zool. 2012;288:1-20.

8. Chulkina M.M., Volodin I.A., Volodina E.V. Individual, intersexual and interbreed variability of barks in the dog Canis familiaris (Carnivora, Canidae). Zoologicheskiy zhurnal = Zoological Journal (Moscow). 2006;85(4):544-555. (in Russian)

9. Cohen J.A., Fox M.W. Vocalizations in wild canids and possible effects of domestication. Behav. Process. 1976;1:77-92.

10. Darden S.K., Dabelsteen T. Ontogeny of swift fox Vulpes velox vocalizations: production, usage and response. Behaviour. 2006;143: 659-681.

11. Fitch W.T. The phonetic potential of nonhuman vocal tracts: Comparative cineradiographic observations of vocalizing animals. Phonetica. 2000;57:205-218.

12. Fitch W.T., Neubauer J., Herzel H. Calls out of chaos: the adaptive significance of nonlinear phenomena in mammalian vocal production. Anim. Behav. 2002;63:407-418.

13. Gogoleva S.S., Volodin I.A., Volodina E.V., Kharlamova A.V., Trut L.N. Kind granddaughters of angry grandmothers: The effect of domestication on vocalization in cross-bred silver foxes. Behav. Process. 2009;81(3):369-375.

14. Gogoleva S.S., Volodin I.A., Volodina E.V., Kharlamova A.V., Trut L.N. Sign and strength of emotional arousal: Vocal correlates of positive and negative attitudes to humans in silver foxes (Vulpes vulpes). Behaviour. 2010a;147:1713-1736.

15. Gogoleva S.S., Volodin I.A., Volodina E.V., Kharlamova A.V., Trut L.N. Vocalization toward conspecifics in silver foxes (Vulpes vulpes) selected for tame or aggressive behavior toward humans. Behav. Process. 2010b;84:547-554.

16. Gogoleva S.S., Volodina E.V., Volodin I.A., Kharlamova A.V., Trut L.N. The gradual vocal responses to human-provoked discomfort in farmed silver foxes. Acta Ethol. 2010c;13(2):75- 85.

17. Gogoleva S.S., Volodin I.A., Volodina E.V., Kharlamova A.V., Trut L.N. Explosive vocal activity for attracting human attention is related to domestication in silver fox. Behav. Process. 2011;86:216-221.

18. Gogoleva S.S., Volodin I.A., Volodina E.V., Kharlamova A.V., Trut L.N. Effects of selection for behavior, human approach mode and sex on vocalization in silver fox. J. Ethol. 2013;31(1):95-100.

19. Gogoleva S.S., Volodin I.A., Volodina E.V., Trut L.N. To bark or not to bark: Vocalization in red foxes selected for tameness or aggressiveness toward humans. Bioacoustics. 2008;18(2):99- 132.

20. Gulevich R.G., Oskina I.N., Shikhevich S.G., Fedorova E.V., Trut L.N. Effect of selection for behavior on pituitary-adrenal axis and proopiomelanocortin gene expression in silver foxes (Vulpes vulpes). Physiol. Behav. 2004;82:513-518.

21. Hare B., Plyusnina I., Ignacio N., Schepina O., Stepika A., Wrangham R., Trut L. Social cognitive evolution in captive foxes is a correlated byproduct of experimental domestication. Curr. Biol. 2005; 16:226-230.

22. Kharlamova A.V., Chase K., Lark K.G., Trut L.N. Variation of skeletal parameters in silver fox (Vulpes vulpes), selected for behavior, and in domestic dog (Canis familiaris). Informatsionnyy vestnik VOGiS = The Herald of Vavilov Society for Geneticists and Breeders. 2008;12(1/2):32-38. (in Russian)

23. Kharlamova A.V., Trut L.N., Carrier D.R., Chase K., Lark K.G. Genetic regulation of canine skeletal traits: trade-offs between the hind limbs and forelimbs in the fox and dog. Integr. Comp. Biol. 2007; 47(3):373-381.

24. Kukekova A.V., Acland G.M., Oskina I.N., Kharlamova A.V., Trut L.N., Chase K., Lark K.G., Erb H.N., Aguirre G.D. The genetics of domesticated behavior in canids: what can dogs and silver foxes tell us about each other. The Dog and it’s Genome. N.Y.: Cold Spring Harbor Laboratory Press, 2006;515-537.

25. Kukekova A.V., Oskina I.N., Kharlamova A.V., Chase K., Temnykh S.V., Johnson J.L., Pivovarova I.V., Shepeleva D.V., Vladimirova A., Semenova T.I., Gulievich R.G., Schikhevich S.G., Graphodatsky A.S., Aguirre G.D., Erb H.N., Lark K.G., Acland G.M., Trut L.N. Fox farm experiment: hunting for behavioral genes. Informatsionnyy vestnik VOGiS = The Herald of Vavilov Society for Geneticists and Breeders. 2008a;12(1/2):50-62.

26. Kukekova A.V., Trut L.N., Chase K., Shepeleva D.V., Vladimirova A.V., Kharlamova A.V., Oskina I.N., Stepika A., Klebanov S., Erb H.N., Acland G.M. Measurement of segregating behaviors in experimental silver fox pedigrees. Behav. Genet. 2008b;38:185-194.

27. Kukekova A.V., Trut L.N., Oskina I.N., Johnson J.L., Temnykh S.V., Kharlamova A.V., Shepeleva D.V., Gulievich R.G., Shikhevich S.G., Graphodatsky A.S., Aguirre G.D., Acland G.M. A meiotic linkage map of the silver fox, aligned and compared to the canine genome. Genome Res. 2007;17:387-399.

28. Kukekova A.V., Trut L.N., Oskina I.N., Kharlamova A.V., Shikhevich S.G., Kirkness E.F., Aguirre G.D., Acland G.M. A marker set for construction of a genetic map of the silver fox (Vulpes vulpes). J. Hered. 2004;95:185-194.

29. Lindberg J., Björnerfeldt S., Bakken M., Vila C., Jazin E., Saetre P. Selection for tameness modulates the expression of heme related genes in silver foxes. Behav. Brain Funct. 2007;3:18. DOI 10.1186/1744-9081-3-18.

30. Lord K., Feinstein M., Coppinger R. Barking and mobbing. Behav. Proc. 2009;81:358-368.

31. McComb K., Taylor A.M., Wilson C., Charlton B.D. The cry embedded within the purr. Curr. Biol. 2009;19:R507-R508.

32. Molnár C., Pongrácz P., Dóka A., Miklósi Á. Can humans discriminate between dogs on the base of the acoustic parameters of barks? Behav. Process. 2006;73:76-83.

33. Monticelli P.F., Ades C. Bioacoustics of domestication: Alarm and courtship calls of wild and domestic cavies. Bioacoustics. 2011; 20(2):169-192.

34. Movchan V.N., Orlova I.N. Determination of informative traits of rhythmically organized vocalizations in the red fox (Vulpes vulpes). Zhurnal evolyutsionnoy biokhimii i fiziologii = Journal of Evolutionary Biochemistry and Physiology.1990;26(3):398-404. (in Russian)

35. Newton-Fisher N., Harris S., White P., Jones G. Structure and function of red fox (Vulpes vulpes) vocalizations. Bioacoustics. 1993;5:1-31.

36. Nicastro N. Perceptual and acoustic evidence for species-level differences in meow vocalizations by domestic cats (Felis catus) and African wild cats (Felis silvestris lybica). J. Comp. Psychol. 2004;118: 287-296.

37. Nicastro N., Owren M.J. Classification of domestic cat (Felis catus) vocalizations by naïve and experienced human listeners. J. Comp. Psychol. 2003;117:44-52.

38. Oskina I.N. Analysis of the functional state of the pituitary-adrenal axis during postnatal development of domesticated silver foxes (Vulpes vulpes). Scientifur. 1996;20:159-161.

39. Oskina I.N., Herbeck Yu.E., Shikhevich S.G., Plyusnina I.Z., Gulevich R.G. Alterations in the hypothalamus-pituitary-adrenal and immune systems during selection of animals for tame behavior. Informatsionnyy vestnik VOGiS = The Herald of Vavilov Society for Geneticists and Breeders. 2008;12(1/2):39-49. (in Russian)

40. Ovsyanikov N.G., Rutovskaya M.V., Menushina I.E., Neprintseva E.S. Social behaviour of Arctic foxes (Alopex lagopus): the vocal repertoire. Zoologicheskiy zhurnal = Zoological Journal (Moscow). 1988;67(9):1371-1380. (in Russian)

41. Plyusnina I., Oskina I., Trut L. An analysis of fear and aggression during early development of behavior in silver foxes (Vulpes vulpes). Appl. Anim. Behav. Sci. 1991;32:253-268.

42. Pongrácz P., Miklósi Á., Molnár C., Csányi V. Human listeners are able to classify dog (Canis familiaris) barks recorded in different situations. J. Comp. Psychol. 2005;119:136-144.

43. Pongrácz P., Molnár C., Miklósi Á. Acoustic parameters of dog barks carry emotional information for humans. Appl. Anim. Behav. Sci. 2006;100:228-240.

44. Popova N., Voitenko N., Kukikov A., Avgustinovich D. Evidence for the involvement of central serotonin in the mechanism of domestication of silver foxes. Pharmacol. Biochem. Behav. 1991;40:751-756.

45. Riede T., Bronson E., Hatzikirou H., Ziberbuhler K. Vocal production mechanisms in a non- human primate: morphological data and a model. J. Human Evol. 2005;48:85-96.

46. Sablin M.V., Khlopachev G.A. The earliest ice age dogs: evidence from Eliseevichi I. Curr. Anthropol. 2002;43:795-799.

47. Safronov O.V., Goltsman M.E., Kruchenkova E.P., Ovsjanikov N.G., Smirin V.M. Akusticheskiy repertuar pestsa [The acoustic repertoire of the Arctic fox]. Ekologicheskie osnovy okhrany i ratsionalnogo ispolzovaniya khishchnykh mlekopitayushchikh [Ecological Frameworks for Conservation, Protection, and Sustainable Use of Predatory Mammals]. Moscow: Nauka Publ., 1979;160-161. (in Russian)

48. Shipley C., Carterette E.C., Buchwald J.S. The effect of articulation on the acoustical structure of feline vocalization. J. Acoust. Soc. Am. 1991;89:902-909.

49. Tchernov E., Valla F.F. Two new dogs, and other Natufian dogs, from the southern Levant. J. Archaeol. Sci. 1997;24:65-95.

50. Tembrock G. Canid vocalizations. Behav. Process. 1976;1:57-75.

51. Trut L.N. Genetika i fenogenetika domestikatsionnogo povedeniya [Genetics and phenogenetics of domesticated behaviour]. Voprosy obshchey genetiki [Problems of General Genetics]. Moscow: Nauka Publ., 1981;323-332. (in Russian)

52. Trut L.N. Early canid domestication: the farm-fox experiment. Am. Sci. 1999;87:160-169.

53. Trut L.N. Problema destabiliziruyushchego otbora v razvitii [Background of the problem of destabilizing selection]. Sovremennye kontseptsii evolyutsionnoy genetiki [Current Concepts of Evolutionary Genetics]. Novosibirsk: Institute of Cytology and Genetics of Siberian Branch of the Russian Academy of Sciences, 2000;7-21. (in Russian)

54. Trut L.N. Domestication of animals as the historical process and as the eхperiment. Informatsionnyy vestnik VOGiS = The Herald of Vavilov Society for Geneticists and Breeders. 2007;11(2):273-289. (in Russian)

55. Trut L.N., Oskina I.N., Kharlamova A.V. Animal evolution during domestication: the domesticated fox as a model. BioEssays. 2009;31: 349-360.

56. Trut L.N., Plyusnina I.Z., Kolesnikova L.A., Kozlova O.N. Interhemispheral neurochemical differences in brains of silver foxes selected for behavior and the problem of directional asymmetry. Russ. J. Genet. 2000;36:776-780.

57. Trut L.N., Plyusninа I.Z., Oskina I.N. An experiment on fox domestication and debatable issues of evolution in the dog. Genetika = Genetics (Moscow). 2004;40(6):794-807. (in Russian)

58. Volodin I.A., Volodina E.V., Filatova O.A. Structure, occurrence, and functional significance of nonlinear phenomena in calls of terrestrial mammals. Zhurnal obshchey biologii = Journal of General Biology. 2005;66(4):346-362. (in Russian)

59. Volodin I.A., Volodina E.V., Filatova O.A. Nonlinear phenomena determine the high structural variability of whines in the domestic dog Canis familiaris (Carnivora, Canidae). Byulleten MOIP. Otdelenie biologii = Bulletin of the Moscow Society of Naturalists. Biological Series. 2007;112(4):11-17. (in Russian)

60. Volodin I.A., Volodina E.V., Gogoleva S.S., Doronina L.O. Signs of emotional arousal in vocalizations of humans and nonhuman mammals. Zhurnal obshchey biologii = Journal of General Biology. 2009;70(3):210-224. (in Russian)

61. Wilden I., Herzel H., Peters G., Tembrock G. Subharmonics, biphonation, and deterministic chaos in mammal vocalization. Bioacoustics. 1998;9:171-196.

62. Yin S. A new perspective on barking in dogs (Canis familiaris). J. Comp. Psychol. 2002;116:189-193.

63. Yin S., McCowan B. Barking in domestic dogs: context specificity and individual identification. Anim. Behav. 2004;68:343-355.

64. Zaytseva A.S., Volodin I.A., Ilchenko O.G., Volodina E.V. Discomfortrelated changes in pup ultrasonic calls of fat-tailed gerbils Pachyuromys duprasi. Bioacoustics. 2017;26:1-13.