vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RAS10.18699/VJ17.262vavilov-1020Research ArticleЭволюционная генетикаEvolutionary genetics«Синдром одомашнивания» в свете геномных данныхRevisiting two hypotheses on the “domestication syndrome” in light of genomic dataУилкинсА. С.WilkinsA. S.wilkins316@btinternet.comИнститут теоретической биологии Берлинского университета им. ГумбольдтаГерманияInstitute of Theoretical Biology, Humboldt Universität zu BerlinGermany201724072017214435442Copyright © Уилкинс А.С., 20172017Уилкинс А.С.Wilkins A.S.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/1020

Доместицированные млекопитающие разных видов имеют общий набор физических и физиологических признаков, которых не было у их диких предков. Совокупность этих признаков, называемая «синдромом одомашнивания», остается загадкой со времен Чарльза Дарвина, открывшего этот феномен. В настоящее время существуют две общие гипотезы, объясняющие это явление, которые отчасти применимы и к другим позвоночным, например рыбам и птицам. Одну из этих гипотез мы называем гипотезой тиреоидных гормонов (THH), а другую – гипотезой клеток нервного гребня (NCCH). Каждая из гипотез приводит к совершенно разным выводам на уровне генетики. Основываясь на анализе последних данных геномных исследований, имеющих отношение к обсуждаемому вопросу, мы пришли к выводу, что более обоснованной выглядит гипотеза NCCH. Тем не менее ряд наблюдений, сделанных на курах, указывает на потенциально важную роль измененного метаболизма тиреоидных гормонов для процесса одомашнивания. Кроме того, недавние исследования указывают на возможность существования дополнительных факторов одомашнивания, оказывающих влияние на приручаемость и социальность и не учитываемых ни одной из рассматриваемых гипотез. Кратко обсуждаются задачи, направленные на выявление генетических основ «синдрома одомашнивания» и особенностей поведения, специфичных для процесса одомашнивания млекопитающих.

Domesticated mammals of many different species share a set of physical and physiological traits that are not displayed by any of their wild progenitors. This suite of traits, now termed the “domestication syndrome” (DS), has been a puzzle since Charles Darwin discovered it. Two general explanations of its basis have been proposed, which in principle, could also apply to other vertebrates, such as fish and birds, whose domesticated varieties show some of its elements. The two ideas are termed here, respectively, the thyroid hormone hypothesis or the THH, and the neural crest cell hypothesis, the NCCH. The two ideas make distinctly different genetic predictions. Here, the current relevant evidence from genomics is evaluated and it is concluded that the NCCH has more support. Nevertheless, one set of observations, from chickens, suggest a potentially important role of altered thyroid metabolism in domestication. In addition, recent studies indicate the possibility of additional genetic factors in domestication, affecting tameness and sociality, that may go beyond either hypothesis. The tasks that lie ahead to fully ascertain the genetic bases of the “domestication syndrome” and the behaviors that characterize mammalian domestication are discussed briefly.

одомашнивание животных«синдром одомашнивания»Чарльз Дарвинсравнительная геномиканеотенияклетки нервного гребняметаболизм тиреоидных гормоновanimal domestication“domestication syndrome”Charles Darwincomparative genomicsneotenyneural crest cellsthyroid metabolism.ReferencesAlbert F., Carlborg O., Plyushina I., Besnier F., Hedwig D., Lautenschläger S., Lorenz D., McIntosh J., Neumann C., Richter H., Zeising C., Kozhemyakina R., Shchepina O., Kratzsch J., Trut L., Teupser D., Thiery J., Schöneberg T., Andersson L., Pääbo S. Genetic architecture of tameness in a rat model of animal domestication. Genetics. 2009;182(2):541-554.Albert F., Carlborg O., Plyushina I., Besnier F., Hedwig D., Lautenschläger S., Lorenz D., McIntosh J., Neumann C., Richter H., Zeising C., Kozhemyakina R., Shchepina O., Kratzsch J., Trut L., Teupser D., Thiery J., Schöneberg T., Andersson L., Pääbo S. Genetic architecture of tameness in a rat model of animal domestication. Genetics. 2009;182(2):541-554.Axelsson E., Ratnakumar A., Arendt M.L., Maqbool K., Webster M.T., Perloski M., Liberg O., Arnemo J.M., Hedhammar A., Lindblad- Toh K. The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature. 2013;495:360-364.Axelsson E., Ratnakumar A., Arendt M.L., Maqbool K., Webster M.T., Perloski M., Liberg O., Arnemo J.M., Hedhammar A., Lindblad- Toh K. The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature. 2013;495:360-364.Behringer C., Deschner T., Murtagh R., Stevens J.M.G., Hohmann G. Age-related changes in thyroid hormone levels of bonobos and chimpanzees indicated heterochrony in development. J. Hum. Evol. 2013;66:83-88.Behringer C., Deschner T., Murtagh R., Stevens J.M.G., Hohmann G. Age-related changes in thyroid hormone levels of bonobos and chimpanzees indicated heterochrony in development. J. Hum. Evol. 2013;66:83-88.Belteky J., Agnavall B., Johnsson M., Wright D., Jensen P. Domestication and tameness: brain gene expression in red junglefowl selected for less fear of humans suggests effects on reproduction and immunology. R. Soc. Open Sci. 2016;3:160033.Belteky J., Agnavall B., Johnsson M., Wright D., Jensen P. Domestication and tameness: brain gene expression in red junglefowl selected for less fear of humans suggests effects on reproduction and immunology. R. Soc. Open Sci. 2016;3:160033.Belyaev D. Domestication, plant and animal. Encyclopaedia Brittanica, Edition 15. Ed. H.H. Benton. Chicago: Encylopaedia Brittanica- Helen Hemingway Benton Publ., 1974.Belyaev D. Domestication, plant and animal. Encyclopaedia Brittanica, Edition 15. Ed. H.H. Benton. Chicago: Encylopaedia Brittanica- Helen Hemingway Benton Publ., 1974.Belyaev D. Destabilizing selection as a factor in domestication. J. Heredity. 1979;70:301-308.Belyaev D. Destabilizing selection as a factor in domestication. J. Heredity. 1979;70:301-308.Benitez-Burraco A., Di Pietro L., Barba M., Lattanzai W. Schizophrenia and human self- domestication: an evolutionary linguistics approach. Brain Behav. Evol. 2017. https://doi.org/10.1159/000468506.Benitez-Burraco A., Di Pietro L., Barba M., Lattanzai W. Schizophrenia and human self- domestication: an evolutionary linguistics approach. Brain Behav. Evol. 2017. https://doi.org/10.1159/000468506.Bronchain O.J., Chesneau A., Monsoro-Burq A.-H., Jolivet P., Pailland E., Scanlan T.S., Demeneix B.A., Sachs L.M., Pollet N. Implication of thyroid hormone signaling in neural crest cells migration: Evidence from thyroid hormone receptor beta knockdown and NH3 antagonist studies. Mol. Cell. Endocrinol. 2017;439:233-246. DOI 10.1016/j.mce.2016.09.007.Bronchain O.J., Chesneau A., Monsoro-Burq A.-H., Jolivet P., Pailland E., Scanlan T.S., Demeneix B.A., Sachs L.M., Pollet N. Implication of thyroid hormone signaling in neural crest cells migration: Evidence from thyroid hormone receptor beta knockdown and NH3 antagonist studies. Mol. Cell. Endocrinol. 2017;439:233-246. DOI 10.1016/j.mce.2016.09.007.Brüne M. On human self-domestication, psychiatry and genetics. Philosophy, Ethics, and Humanities in Medicine. 2007;2:21-29.Brüne M. On human self-domestication, psychiatry and genetics. Philosophy, Ethics, and Humanities in Medicine. 2007;2:21-29.Carneiro M., Rubin C.-J., di Palma F., Albert F.W., Alifoldi J. Rabbit genome analysis reveals a polygenic basis for phenotypic change during domestication. Science. 2014;345:1074-1079.Carneiro M., Rubin C.-J., di Palma F., Albert F.W., Alifoldi J. Rabbit genome analysis reveals a polygenic basis for phenotypic change during domestication. Science. 2014;345:1074-1079.Carneiro M., Piorno V., Rubin C.-J., Alves J.M., Ferrand N., Alves P.C., Andersson L. Candidate genes underlying heritable differences in reproductive seasonality between wild and domestic rabbits. Anim. Genetics. 2015;46:418-425.Carneiro M., Piorno V., Rubin C.-J., Alves J.M., Ferrand N., Alves P.C., Andersson L. Candidate genes underlying heritable differences in reproductive seasonality between wild and domestic rabbits. Anim. Genetics. 2015;46:418-425.Crockford S. Animal domestication and heterochronic speciation. Human Evolution Through Developmental Change. Eds. N. Minugh- Purvis, K.J. McNamara. Baltimore: Johns Hopkins Univ. Press, 2002;122-153.Crockford S. Animal domestication and heterochronic speciation. Human Evolution Through Developmental Change. Eds. N. Minugh- Purvis, K.J. McNamara. Baltimore: Johns Hopkins Univ. Press, 2002;122-153.Darwin C. The Variation of Animals and Plants under Domestication. London: John Murray, 1868.Darwin C. The Variation of Animals and Plants under Domestication. London: John Murray, 1868.Diamond J. Guns, Germs and Steel. London: Vintage Books, 1999.Diamond J. Guns, Germs and Steel. London: Vintage Books, 1999.Francis R.C. Domesticated: Evolution in a Man-Made World. W.W. Norton, New York, 2015.Francis R.C. Domesticated: Evolution in a Man-Made World. W.W. Norton, New York, 2015.Frantz L.A.F., Mullin V.E., Pionnier-Capitan M., Lebrasseur O., Ollivier M. Genomic and archaeological evidence suggests a dual origin of domestic dogs. Science. 2016;352:1228-1231.Frantz L.A.F., Mullin V.E., Pionnier-Capitan M., Lebrasseur O., Ollivier M. Genomic and archaeological evidence suggests a dual origin of domestic dogs. Science. 2016;352:1228-1231.Glazko V., Zybaylov B., Glazko T. Domestication and genome evolution. Int. J. Genet. Genom. 2014;2:47-56.Glazko V., Zybaylov B., Glazko T. Domestication and genome evolution. Int. J. Genet. Genom. 2014;2:47-56.Hammer K. Das domestiationsyndrom. Kulturpflanz. 1984;32:11-34.Hammer K. Das domestiationsyndrom. Kulturpflanz. 1984;32:11-34.Hare B., Wobber V., Wrangham R. The self-domestication hypothesis: bonobo psychology evolved due to selection against aggression. Anim. Behav. 2012;83:573-585.Hare B., Wobber V., Wrangham R. The self-domestication hypothesis: bonobo psychology evolved due to selection against aggression. Anim. Behav. 2012;83:573-585.Karlsson A.-C., Svemer F., Eriksson J., Darras V.M., Andersson L., Jensen P. The effect of a mutation in the thyroid stimulating hormone receptor (TSHR) on development, behavior and TH levels in domesticated chickens. PLoS ONE. 2015. DOI 101371/journal.pone.0129040.Karlsson A.-C., Svemer F., Eriksson J., Darras V.M., Andersson L., Jensen P. The effect of a mutation in the thyroid stimulating hormone receptor (TSHR) on development, behavior and TH levels in domesticated chickens. PLoS ONE. 2015. DOI 101371/journal.pone.0129040.Karlsson A.-C., Fallahshahroudi A., Johnsen H., Hagenblad J., Wright D., Andersson L., Jensen P. A domestication-related mutation in the thyroid stimulating hormone receptor gene (TSHR) modulates photoperiodic response and reproduction in chickens. Gen. Comp. Endocrinol. 2016;228:69-78.Karlsson A.-C., Fallahshahroudi A., Johnsen H., Hagenblad J., Wright D., Andersson L., Jensen P. A domestication-related mutation in the thyroid stimulating hormone receptor gene (TSHR) modulates photoperiodic response and reproduction in chickens. Gen. Comp. Endocrinol. 2016;228:69-78.Larson G., Piperno D.R., Allaby R.G., Purugganan M.D., Andersson L., Arroyo-Kalin M., Barton L., Climer Vigueira C., Denham T., Dobney K., Doust A.N., Gepts P., Gilbert M.T.P., Gremillion K.J., Lucas L., Lukens L., Marshall F.B., Olsen K.M., Pires J.C., Richerson P.J., Rubio de Casas R., Sanjur O.I., Thomas M.G., Fuller D.Q. Current perspectives and the future of domestication studies. Proc. Natl. Acad. Sci. USA. 2014;111(17):6139-6146.Larson G., Piperno D.R., Allaby R.G., Purugganan M.D., Andersson L., Arroyo-Kalin M., Barton L., Climer Vigueira C., Denham T., Dobney K., Doust A.N., Gepts P., Gilbert M.T.P., Gremillion K.J., Lucas L., Lukens L., Marshall F.B., Olsen K.M., Pires J.C., Richerson P.J., Rubio de Casas R., Sanjur O.I., Thomas M.G., Fuller D.Q. Current perspectives and the future of domestication studies. Proc. Natl. Acad. Sci. USA. 2014;111(17):6139-6146.Leach H.M. Human domestication reconsidered. Curr. Anthrop. 2003; 43:349-368.Leach H.M. Human domestication reconsidered. Curr. Anthrop. 2003; 43:349-368.Librado P., Gamba C., Gaunitz C., Der Sarkissian C., Pruvost M., Albrechtsen A., Fages A., Khan N., Schubert M., Jagannathan V., Serres A., Kuderna L.F.K., Povolotskaya I., Seguin- Orlando S., Lepetz S., Neuditschko M., Theves C., Alquaraishi S., Alfarhan A.H., Al-Rasheid K., Rieder S., Samashev Z., Francfort H.P., Beneccke N., Hofreiter M., Ludwig A., Keyser C., Marques-Bonet T., Ludes B., Crubezy E., Leeb T., Willerslev E., Orlando L. Ancient genomic changes associated with domestication of the horse. Science. 2017;356:442-445.Librado P., Gamba C., Gaunitz C., Der Sarkissian C., Pruvost M., Albrechtsen A., Fages A., Khan N., Schubert M., Jagannathan V., Serres A., Kuderna L.F.K., Povolotskaya I., Seguin- Orlando S., Lepetz S., Neuditschko M., Theves C., Alquaraishi S., Alfarhan A.H., Al-Rasheid K., Rieder S., Samashev Z., Francfort H.P., Beneccke N., Hofreiter M., Ludwig A., Keyser C., Marques-Bonet T., Ludes B., Crubezy E., Leeb T., Willerslev E., Orlando L. Ancient genomic changes associated with domestication of the horse. Science. 2017;356:442-445.Montague M., Li G., Gandolfi B., Khan R., Aken B., Searle S.M.J., Minx P., Hillier L., Kolboldt D.C., Davis B.W., Driscoll C.A., Barr C., Blackistone K., Quilez J., Lorente-Galdos B., Marques- Bonet T., Alkan C., Thomas G.W.C., Hahn M.W., Menotti-Raymond M., O’Brien S.J., Wilson R.K., Lyons L.A., Murphy W.J., Warren W.C. Comparative analysis of the domestic cat genome reveals genetic signatures underlying feline biology and domestication. Proc. Natl. Acad. Sci. USA. 2014;111:17230-17236.Montague M., Li G., Gandolfi B., Khan R., Aken B., Searle S.M.J., Minx P., Hillier L., Kolboldt D.C., Davis B.W., Driscoll C.A., Barr C., Blackistone K., Quilez J., Lorente-Galdos B., Marques- Bonet T., Alkan C., Thomas G.W.C., Hahn M.W., Menotti-Raymond M., O’Brien S.J., Wilson R.K., Lyons L.A., Murphy W.J., Warren W.C. Comparative analysis of the domestic cat genome reveals genetic signatures underlying feline biology and domestication. Proc. Natl. Acad. Sci. USA. 2014;111:17230-17236.Pendleton A.L., Shen F., Taravella A.M., Emery S., Veeramah K.R., Boyko A.R., Kidd J.M. Selective sweep analysis using village dogs highlights the pivotal role of the neural crest in dog domestication. BioRxiv. 2017. dx.doi.org/10.1101/118794.Pendleton A.L., Shen F., Taravella A.M., Emery S., Veeramah K.R., Boyko A.R., Kidd J.M. Selective sweep analysis using village dogs highlights the pivotal role of the neural crest in dog domestication. BioRxiv. 2017. dx.doi.org/10.1101/118794.Persson M.E., Wright D., Roth L.S.V., Batakis P., Jensen P. Genomic regions associated with interspecific communication in dogs contain genes related to human social disorders. Sci. Rep. 2016;6:33439. DOI 10.1038/srep 33439.Persson M.E., Wright D., Roth L.S.V., Batakis P., Jensen P. Genomic regions associated with interspecific communication in dogs contain genes related to human social disorders. Sci. Rep. 2016;6:33439. DOI 10.1038/srep 33439.Price E.O. Behavioral development in animals undergoing domestication. Appl. Anim. Behav. Sci. 1999;65:245-271.Price E.O. Behavioral development in animals undergoing domestication. Appl. Anim. Behav. Sci. 1999;65:245-271.Rubin C.-J., Megens H.-J., Martinez Barrio A., Maqbool K., Sayyab S., Schwochow D., Wang C., Carlborg Ö., Jern P., Jørgensen C.B., Archibald A.L., Fredholm M., Groenen M.A.M., Andersson L. Strong signatures of selection in the domestic pig genome. Proc. Natl. Acad. Sci. USA. 2012;48:19529-19536.Rubin C.-J., Megens H.-J., Martinez Barrio A., Maqbool K., Sayyab S., Schwochow D., Wang C., Carlborg Ö., Jern P., Jørgensen C.B., Archibald A.L., Fredholm M., Groenen M.A.M., Andersson L. Strong signatures of selection in the domestic pig genome. Proc. Natl. Acad. Sci. USA. 2012;48:19529-19536.Sanchez-Villagra M.R., Geiger M., Schneider R.A. The taming of the neural crest: a developmental perspective on the origins of morphological co-variation in domesticated mammals. R. Soc. Open Sci. 2016;3:160107.Sanchez-Villagra M.R., Geiger M., Schneider R.A. The taming of the neural crest: a developmental perspective on the origins of morphological co-variation in domesticated mammals. R. Soc. Open Sci. 2016;3:160107.Schubert M., Jonsson H., Chang D., Sarkissian C.D., Ermini L., Ginolhac A., Albrechtsen A. Prehistoric genomes reveal the genetic foundation and cost of horse domestication. Proc. Natl. Acad. Sci. USA. 2014;111(52):e5661-e5669. DOI 10.1073/pnas.1416991111.Schubert M., Jonsson H., Chang D., Sarkissian C.D., Ermini L., Ginolhac A., Albrechtsen A. Prehistoric genomes reveal the genetic foundation and cost of horse domestication. Proc. Natl. Acad. Sci. USA. 2014;111(52):e5661-e5669. DOI 10.1073/pnas.1416991111.Theofanopolou C., Gastaldon S., O’Rourke R., Samuels B.D., Messner A., Martins P.T., Delogu F., Alamri S., Boeckx C. Comparative genomic evidence for self-domestication in Homo sapiens. BioRxiv. 2017. doi.org/10.1101/125799.Theofanopolou C., Gastaldon S., O’Rourke R., Samuels B.D., Messner A., Martins P.T., Delogu F., Alamri S., Boeckx C. Comparative genomic evidence for self-domestication in Homo sapiens. BioRxiv. 2017. doi.org/10.1101/125799.Trut L. Early canid domestication: the farm-fox experiment. Am. Scientist. 1999;87:160-168.Trut L. Early canid domestication: the farm-fox experiment. Am. Scientist. 1999;87:160-168.Trut L., Oskina I., Kharlamova A. Animal evolution during domestication: the domesticated fox as a model. BioEssays. 2009;31:349-360.Trut L., Oskina I., Kharlamova A. Animal evolution during domestication: the domesticated fox as a model. BioEssays. 2009;31:349-360.Vigne J.D. The origins of animal domestication and husbandry: a major change in the history of humanity and the biosphere. Comptes Rendues Biologies. 2011;334(3):171-181.Vigne J.D. The origins of animal domestication and husbandry: a major change in the history of humanity and the biosphere. Comptes Rendues Biologies. 2011;334(3):171-181.Wilkins A.S. Epigenetic inheritance: Where does the field stand today? What do we still need to know? Transformations of Lamarckism: From Subtle Fluids to Molecular Biology. Eds. S.B. Gissis, E. Jablonka. Cambridge: MIT Press, 2011;389-393.Wilkins A.S. Epigenetic inheritance: Where does the field stand today? What do we still need to know? Transformations of Lamarckism: From Subtle Fluids to Molecular Biology. Eds. S.B. Gissis, E. Jablonka. Cambridge: MIT Press, 2011;389-393.Wilkins A.S., Wrangham R., Fitch T. The “domestication syndrome” in mammals: a unified explanation based on neural crest cell behavior and genetics. Genetics. 2014;197:795-808.Wilkins A.S., Wrangham R., Fitch T. The “domestication syndrome” in mammals: a unified explanation based on neural crest cell behavior and genetics. Genetics. 2014;197:795-808.

The authors declare that there are no conflicts of interest present.