Movatterモバイル変換


[0]ホーム

URL:


Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Advertisement

Nature Reviews Genetics
  • Review Article
  • Published:

Animal domestication in the era of ancient genomics

Nature Reviews Geneticsvolume 21pages449–460 (2020)Cite this article

Subjects

Abstract

The domestication of animals led to a major shift in human subsistence patterns, from a hunter–gatherer to a sedentary agricultural lifestyle, which ultimately resulted in the development of complex societies. Over the past 15,000 years, the phenotype and genotype of multiple animal species, such as dogs, pigs, sheep, goats, cattle and horses, have been substantially altered during their adaptation to the human niche. Recent methodological innovations, such as improved ancient DNA extraction methods and next-generation sequencing, have enabled the sequencing of whole ancient genomes. These genomes have helped reconstruct the process by which animals entered into domestic relationships with humans and were subjected to novel selection pressures. Here, we discuss and update key concepts in animal domestication in light of recent contributions from ancient genomics.

This is a preview of subscription content,access via your institution

Access options

Access through your institution

Access Nature and 54 other Nature Portfolio journals

Get Nature+, our best-value online-access subscription

9,800 Yen / 30 days

cancel any time

Subscription info for Japanese customers

We have a dedicated website for our Japanese customers. Please go tonatureasia.com to subscribe to this journal.

Buy this article

  • Purchase on SpringerLink
  • Instant access to the full article PDF.

¥ 4,980

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Increase in the number of published ancient genomes for domesticated animal species and their wild relatives.
Fig. 2: Influence of ancient genomics on models of animal domestication.
Fig. 3: Major dispersals of domesticated animals uncovered by ancient genomics.
Fig. 4: Spatio-temporal pattern of admixture between cattle and zebu.
Fig. 5: Frequency of alleles underlying modern phenotypes in key domestic animal species.

Similar content being viewed by others

References

  1. Zeder, M. A. The domestication of animals.J. Anthropol. Res.68, 161–190 (2012).

    Article  Google Scholar 

  2. Vigne, J.-D. The origins of animal domestication and husbandry: a major change in the history of humanity and the biosphere.C. R. Biol.334, 171–181 (2011).

    Article PubMed  Google Scholar 

  3. Larson, G. et al. Rethinking dog domestication by integrating genetics, archeology, and biogeography.Proc. Natl Acad. Sci. USA109, 8878–8883 (2012).

    Article CAS PubMed PubMed Central  Google Scholar 

  4. Darwin, C.The Variation of Animals and Plants Under Domestication (John Murray, 1868).

  5. McHugo, G. P., Dover, M. J. & MacHugh, D. E. Unlocking the origins and biology of domestic animals using ancient DNA and paleogenomics.BMC Biol.17, 98 (2019).

    Article CAS PubMed PubMed Central  Google Scholar 

  6. Conolly, J. et al. Meta-analysis of zooarchaeological data from SW Asia and SE Europe provides insight into the origins and spread of animal husbandry.J. Archaeol. Sci.38, 538–545 (2011).

    Article  Google Scholar 

  7. Vigne, J.-D. inThe Neolithic Demographic Transition and its Consequences (eds Bocquet-Appel, J.-P. & Bar-Yosef, O.) 179–205 (Springer, 2008).

  8. Ervynck, A., Dobney, K., Hongo, H. & Meadow, R. Born free? New evidence for the status of ‘Sus scrofa’ at Neolithic Çayönü Tepesi (Southeastern Anatolia, Turkey).Paléorient27, 47–73 (2001).

    Article  Google Scholar 

  9. Payne, S. Kill-off patterns in sheep and goats: the mandibles from Aşvan kale.Anatol. Stud.23, 281–303 (1973).

    Article  Google Scholar 

  10. Balasse, M. et al. Wild, domestic and feral? Investigating the status of suids in the Romanian Gumelniţa (5th mil. cal BC) with biogeochemistry and geometric morphometrics.J. Anthropol. Archaeol.42, 27–36 (2016).

    Article  Google Scholar 

  11. Pitulko, V. V. & Kasparov, A. K. Archaeological dogs from the Early Holocene Zhokhov site in the Eastern Siberian Arctic.J. Archaeol. Sci. Rep.13, 491–515 (2017).

    Google Scholar 

  12. Olsen, S. L. Early horse domestication: weighing the evidence.BAR. Int. Ser.1560, 81 (2006).

    Google Scholar 

  13. Larson, G. et al. Worldwide phylogeography of wild boar reveals multiple centers of pig domestication.Science307, 1618–1621 (2005).

    Article CAS PubMed  Google Scholar 

  14. Luikart, G. et al. Multiple maternal origins and weak phylogeographic structure in domestic goats.Proc. Natl Acad. Sci. USA98, 5927–5932 (2001).

    Article CAS PubMed PubMed Central  Google Scholar 

  15. Naderi, S. et al. The goat domestication process inferred from large-scale mitochondrial DNA analysis of wild and domestic individuals.Proc. Natl Acad. Sci. USA105, 17659–17664 (2008).

    Article CAS PubMed PubMed Central  Google Scholar 

  16. Pedrosa, S. et al. Evidence of three maternal lineages in Near Eastern sheep supporting multiple domestication events.Proc. Biol. Sci.272, 2211–2217 (2005).

    PubMed PubMed Central  Google Scholar 

  17. Vilà, C. et al. Widespread origins of domestic horse lineages.Science291, 474–477 (2001).

    Article PubMed  Google Scholar 

  18. Eriksson, J. et al. Identification of the yellow skin gene reveals a hybrid origin of the domestic chicken.PLoS Genet.4, e1000010 (2008).

    Article PubMed PubMed Central CAS  Google Scholar 

  19. Wright, D. Article commentary: the genetic architecture of domestication in animals.Bioinform. Biol. Insights9S4, BBI.S28902 (2015).

    Article  Google Scholar 

  20. Shannon, L. M. et al. Genetic structure in village dogs reveals a Central Asian domestication origin.Proc. Natl Acad. Sci. USA112, 13639–13644 (2015).

    Article CAS PubMed PubMed Central  Google Scholar 

  21. Wang, G.-D. et al. Out of southern East Asia: the natural history of domestic dogs across the world.Cell Res.26, 21–33 (2016).

    Article PubMed  Google Scholar 

  22. Pang, J.-F. et al. mtDNA data indicate a single origin for dogs south of Yangtze River, less than 16,300 years ago, from numerous wolves.Mol. Biol. Evol.26, 2849–2864 (2009).

    Article CAS PubMed PubMed Central  Google Scholar 

  23. Higuchi, R., Bowman, B., Freiberger, M., Ryder, O. A. & Wilson, A. C. DNA sequences from the quagga, an extinct member of the horse family.Nature312, 282–284 (1984).

    Article CAS PubMed  Google Scholar 

  24. Pääbo, S. Ancient DNA: extraction, characterization, molecular cloning, and enzymatic amplification.Proc. Natl Acad. Sci. USA86, 1939–1943 (1989).

    Article PubMed PubMed Central  Google Scholar 

  25. Hagelberg, E. et al. Analysis of ancient bone DNA: techniques and applications.Philos. Trans. R. Soc. Lond. B Biol. Sci.333, 399–407 (1991).

    Article CAS PubMed  Google Scholar 

  26. Römpler, H. et al. The rise and fall of the chemoattractant receptor GPR33.J. Biol. Chem.280, 31068–31075 (2005).

    Article PubMed CAS  Google Scholar 

  27. Hofreiter, M., Serre, D., Poinar, H. N., Kuch, M. & Pääbo, S. Ancient DNA.Nat. Rev. Genet.2, 353–359 (2001).

    Article CAS PubMed  Google Scholar 

  28. Gilbert, M. T. P., Bandelt, H.-J., Hofreiter, M. & Barnes, I. Assessing ancient DNA studies.Trends Ecol. Evol.20, 541–544 (2005).

    Article PubMed  Google Scholar 

  29. Goodwin, S., McPherson, J. D. & McCombie, W. R. Coming of age: ten years of next-generation sequencing technologies.Nat. Rev. Genet.17, 333–351 (2016).

    Article CAS PubMed  Google Scholar 

  30. Rasmussen, M. et al. Ancient human genome sequence of an extinct Palaeo-Eskimo.Nature463, 757–762 (2010).

    Article CAS PubMed PubMed Central  Google Scholar 

  31. Green, R. E. et al. A draft sequence of the Neandertal genome.Science328, 710–722 (2010).

    Article CAS PubMed PubMed Central  Google Scholar 

  32. Orlando, L., Gilbert, M. T. P. & Willerslev, E. Reconstructing ancient genomes and epigenomes.Nat. Rev. Genet.16, 395–408 (2015).This paper presents a comprehensive review of the techniques for extraction and sequencing of ancient DNA.

    Article CAS PubMed  Google Scholar 

  33. Haak, W. et al. Massive migration from the steppe was a source for Indo-European languages in Europe.Nature522, 207–211 (2015).

    Article CAS PubMed PubMed Central  Google Scholar 

  34. Albrechtsen, A., Nielsen, F. C. & Nielsen, R. Ascertainment biases in SNP chips affect measures of population divergence.Mol. Biol. Evol.27, 2534–2547 (2010).

    Article CAS PubMed PubMed Central  Google Scholar 

  35. Boessenkool, S. et al. Combining bleach and mild predigestion improves ancient DNA recovery from bones.Mol. Ecol. Resour.17, 742–751 (2017).

    Article CAS PubMed  Google Scholar 

  36. Gansauge, M.-T. & Meyer, M. Single-stranded DNA library preparation for the sequencing of ancient or damaged DNA.Nat. Protoc.8, 737–748 (2013).

    Article PubMed CAS  Google Scholar 

  37. Gansauge, M.-T. et al. Single-stranded DNA library preparation from highly degraded DNA using T4 DNA ligase.Nucleic Acids Res.45, e79 (2017).

    Article CAS PubMed PubMed Central  Google Scholar 

  38. Briggs, A. W. et al. Removal of deaminated cytosines and detection of in vivo methylation in ancient DNA.Nucleic Acids Res.38, e87 (2010).

    Article PubMed CAS  Google Scholar 

  39. Rohland, N., Harney, E., Mallick, S., Nordenfelt, S. & Reich, D. Partial uracil–DNA-glycosylase treatment for screening of ancient DNA.Philos. Trans. R. Soc. Lond. B Biol. Sci.370, 20130624 (2015).

    Article PubMed PubMed Central CAS  Google Scholar 

  40. Gamba, C. et al. Genome flux and stasis in a five millennium transect of European prehistory.Nat. Commun.5, 5257 (2014).This paper identifies the petrous temporal bone as the best reservoir of preserved ancient DNA in human remains — a finding that extends to archaeological specimens of domesticated animals and that enables the frequent recovery of whole-genome sequences using shotgun sequencing.

    Article CAS PubMed  Google Scholar 

  41. Verdugo, M. P. et al. Ancient cattle genomics, origins, and rapid turnover in the Fertile Crescent.Science365, 173–176 (2019).This paper presents genome data from ancient Near Eastern cattle and aurochs showing introgression of local aurochs into both early European and Levantine cattle populations. A major shift in genomes occurred ~4,000 years ago, with widespread introgression of zebu ancestry from the East, possibly linked to multi-century drought.

    Article CAS PubMed  Google Scholar 

  42. Daly, K. G. et al. Ancient goat genomes reveal mosaic domestication in the Fertile Crescent.Science361, 85–88 (2018).This study is the first genome-wide investigation of ancient variation in a Fertile Crescent domesticate, the goat, and clearly shows the mosaic nature of domestication via Neolithic Iranian, Anatolian and Levantine goat populations and their asymmetrical relationships to pre-domestication wild genomes. The study also shows 8,000-year-old evidence for selection of genes linked to pigmentation and other traits.

    Article CAS PubMed  Google Scholar 

  43. Frantz, L. A. F. et al. Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe.Proc. Natl Acad. Sci. USA116, 17231–17238 (2019).This paper reveals that the Near Eastern ancestry in the genomes of European domestic pigs, which is associated with the first domestic pigs that were introduced into Europe around 8,000 years ago from the Near East, almost entirely disappeared over 3,000 years ago as a result of interbreeding with local wild boars.

    Article CAS PubMed PubMed Central  Google Scholar 

  44. Colledge, S., Conolly, J., Dobney, K., Manning, K. & Shennan, S.Origins and Spread of Domestic Animals in Southwest Asia and Europe (Left Coast, 2013).

  45. Frantz, L. et al. The evolution of Suidae.Annu. Rev. Anim. Biosci.4, 61–85 (2016).

    Article PubMed  Google Scholar 

  46. Helmer, D., Gourichon, L., Monchot, H., Peters, J. & Segui, M. S. inThe First Steps of Animal Domestication (eds D. Vigne, J., Peters, J. & Helmer, D.). 86–95 (Oxbow Books, 2005).

  47. Hongo, H., Pearson, J., Öksüz, B. & Ilgezdi, G. The process of ungulate domestication at Cayönü, Southeastern Turkey: a multidisciplinary approach focusing onBos sp. andCervus elaphus.Anthropozoologica44, 63–78 (2009).

    Article  Google Scholar 

  48. Perri, A. A wolf in dog’s clothing: initial dog domestication and Pleistocene wolf variation.J. Archaeol. Sci.68, 1–4 (2016).

    Article  Google Scholar 

  49. Drake, A. G., Coquerelle, M. & Colombeau, G. 3D morphometric analysis of fossil canid skulls contradicts the suggested domestication of dogs during the late Paleolithic.Sci. Rep.5, 8299 (2015).

    Article CAS PubMed PubMed Central  Google Scholar 

  50. Outram, A. K. et al. The earliest horse harnessing and milking.Science323, 1332–1335 (2009).

    Article CAS PubMed  Google Scholar 

  51. Frantz, L. A. F. et al. Genomic and archaeological evidence suggest a dual origin of domestic dogs.Science352, 1228–1231 (2016).This paper presents the first analysis of an ancient dog genome. Combined with a comprehensive archaeological survey, the authors argue for a dual origin of domestic dogs.

    Article CAS PubMed  Google Scholar 

  52. Freedman, A. H. et al. Genome sequencing highlights the dynamic early history of dogs.PLoS Genet.10, e1004016 (2014).

    Article PubMed PubMed Central CAS  Google Scholar 

  53. Warmuth, V. et al. Reconstructing the origin and spread of horse domestication in the Eurasian steppe.Proc. Natl Acad. Sci. USA109, 8202–8206 (2012).

    Article CAS PubMed PubMed Central  Google Scholar 

  54. The Bovine Genome Sequencing and Analysis Consortium. et al. The genome sequence of taurine cattle: a window to ruminant biology and evolution.Science324, 522–528 (2009).

    Article PubMed Central CAS  Google Scholar 

  55. Fages, A. et al. Tracking five millennia of horse management with extensive ancient genome time series.Cell177, 1419–1435.e31 (2019).This paper represents a milestone in ancient animal genomics, with the sequencing of over 120 ancient horse genomes. The authors draw multiple key conclusions related to the genetic make-up of modern domestic horses and the fitness cost of modern artificial selection.

    Article CAS PubMed PubMed Central  Google Scholar 

  56. Gaunitz, C. et al. Ancient genomes revisit the ancestry of domestic and Przewalski’s horses.Science360, 111–114 (2018).This study uses ancient horse genomes to show that the Botai horses, which are thought to be the first domestic horses, are not related to modern horses but instead form a lineage that is now almost extinct. The sole surviving representative of this lineage is the modern Przewalski’s horse, which was thought to be the last wild horse but is in fact the descendant of an ancient domesticated population.

    Article CAS PubMed  Google Scholar 

  57. Botigué, L. R. et al. Ancient European dog genomes reveal continuity since the Early Neolithic.Nat. Commun.8, 16082 (2017).This paper describes the analysis of two newly sequenced Neolithic dog genomes from Germany, which revealed that there was no population replacement in European dogs during the Neolithic Age as predicted by Frantz et al. (Science, 2016), contradicting the hypothesis that dogs were domesticated more than once.

    Article PubMed PubMed Central CAS  Google Scholar 

  58. Ní Leathlobhair, M. et al. The evolutionary history of dogs in the Americas.Science361, 81–85 (2018).This study shows that American dogs are the descendants of dogs that dispersed with humans from Siberia into the Americas. Analyses of these genomes revealed that this ancient population of dogs almost completely disappeared after the arrival of Europeans and that the last remnant of this lineage is the genome of the canine transmissible venereal tumour, a contagious cancer clone.

    Article PubMed CAS  Google Scholar 

  59. Leonard, J. A. et al. Ancient DNA evidence for Old World origin of New World dogs.Science298, 1613–1616 (2002).

    Article CAS PubMed  Google Scholar 

  60. Frantz, L. A. F. & Larson, G. inHybrid Communities (eds Stépanoff, C. & Vigne, J.-D.) 23–37 (Routledge, 2018).

  61. Larson, G. & Burger, J. A population genetics view of animal domestication.Trends Genet.29, 197–205 (2013).

    Article CAS PubMed  Google Scholar 

  62. Park, S. D. E. et al. Genome sequencing of the extinct Eurasian wild aurochs,Bos primigenius, illuminates the phylogeography and evolution of cattle.Genome Biol.16, 234 (2015).This paper reports the first ancient cattle genome sequence. Analyses of this Mesolithic British auroch nuclear genome show that although there had been almost no trace found of European auroch mtDNA in modern cattle, male-mediated wild introgression had occurred within Europe.

    Article PubMed PubMed Central CAS  Google Scholar 

  63. Frantz, L. A. F. et al. Evidence of long-term gene flow and selection during domestication from analyses of Eurasian wild and domestic pig genomes.Nat. Genet.47, 1141–1148 (2015).This paper reveals that extensive gene flow between wild and domestic populations took place during the evolutionary history of pigs and hypothesizes that an ‘island of domestication’ exists in the genome of domestic animals.

    Article CAS PubMed  Google Scholar 

  64. Skoglund, P., Ersmark, E., Palkopoulou, E. & Dalén, L. Ancient wolf genome reveals an early divergence of domestic dog ancestors and admixture into high-latitude breeds.Curr. Biol.25, 1515–1519 (2015).This paper reports the first genome-wide data retrieved from an ancient canid and shows that there was gene flow between arctic dogs and a now extinct population of Siberian wolf.

    Article CAS PubMed  Google Scholar 

  65. Marshall, F. B., Dobney, K., Denham, T. & Capriles, J. M. Evaluating the roles of directed breeding and gene flow in animal domestication.Proc. Natl Acad. Sci. USA111, 6153–6158 (2014).

    Article CAS PubMed PubMed Central  Google Scholar 

  66. Schubert, M. et al. Prehistoric genomes reveal the genetic foundation and cost of horse domestication.Proc. Natl Acad. Sci. USA111, E5661–E5669 (2014).

    CAS PubMed PubMed Central  Google Scholar 

  67. Turner, T. L., Hahn, M. W. & Nuzhdin, S. V. Genomic islands of speciation inAnopheles gambiae.PLoS Biol.3, e285 (2005).

    Article PubMed PubMed Central CAS  Google Scholar 

  68. Briggs, W. H., McMullen, M. D., Gaut, B. S. & Doebley, J. Linkage mapping of domestication loci in a large maize–teosinte backcross resource.Genetics177, 1915–1928 (2007).

    Article PubMed PubMed Central  Google Scholar 

  69. Trut, L. Early canid domestication: the Farm-Fox Experiment Foxes bred for tamability in a 40-year experiment exhibit remarkable transformations that suggest an interplay between behavioral genetics and development.Am. Sci.87, 160–169 (1999).

    Article  Google Scholar 

  70. Lord, K. A., Larson, G., Coppinger, R. P. & Karlsson, E. K. The history of farm foxes undermines the animal domestication syndrome.Trends Ecol. Evol.35, 125–136 (2020).

    Article PubMed  Google Scholar 

  71. Librado, P. et al. Ancient genomic changes associated with domestication of the horse.Science356, 442–445 (2017).

    Article CAS PubMed  Google Scholar 

  72. Pendleton, A. L. et al. Comparison of village dog and wolf genomes highlights the role of the neural crest in dog domestication.BMC Biol.16, 64 (2018).

    Article PubMed PubMed Central CAS  Google Scholar 

  73. Marsden, C. D. et al. Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs.Proc. Natl Acad. Sci. USA113, 152–157 (2016).

    Article CAS PubMed  Google Scholar 

  74. MacLeod, I. M., Larkin, D. M., Lewin, H. A., Hayes, B. J. & Goddard, M. E. Inferring demography from runs of homozygosity in whole-genome sequence, with correction for sequence errors.Mol. Biol. Evol.30, 2209–2223 (2013).

    Article CAS PubMed PubMed Central  Google Scholar 

  75. Carneiro, M. et al. Rabbit genome analysis reveals a polygenic basis for phenotypic change during domestication.Science345, 1074–1079 (2014).

    Article CAS PubMed PubMed Central  Google Scholar 

  76. Allaby, R. G., Ware, R. L. & Kistler, L. A re-evaluation of the domestication bottleneck from archaeogenomic evidence.Evol. Appl.12, 29–37 (2019).

    Article PubMed  Google Scholar 

  77. Bosse, M. et al. Regions of homozygosity in the porcine genome: consequence of demography and the recombination landscape.PLoS Genet.8, e1003100 (2012).

    Article CAS PubMed PubMed Central  Google Scholar 

  78. Bollongino, R. et al. Modern taurine cattle descended from small number of near-eastern founders.Mol. Biol. Evol.29, 2101–2104 (2012).

    Article CAS PubMed  Google Scholar 

  79. Murray, C., Huerta-Sanchez, E., Casey, F. & Bradley, D. G. Cattle demographic history modelled from autosomal sequence variation.Philos. Trans. R. Soc. Lond. B Biol. Sci.365, 2531–2539 (2010).

    Article CAS PubMed PubMed Central  Google Scholar 

  80. Kristiansen, K.The Rise of Bronze Age Society: Travels, Transmissions and Transformations (Cambridge University Press, 2005).

  81. Allentoft, M. E. et al. Population genomics of Bronze Age Eurasia.Nature522, 167–172 (2015).

    Article CAS PubMed  Google Scholar 

  82. Damgaard, P. et al. 137 ancient human genomes from across the Eurasian steppes.Nature557, 369–374 (2018).

    Article CAS PubMed  Google Scholar 

  83. Jeong, C. et al. Bronze Age population dynamics and the rise of dairy pastoralism on the eastern Eurasian steppe.Proc. Natl Acad. Sci. USA115, E11248–E11255 (2018).

    Article CAS PubMed PubMed Central  Google Scholar 

  84. Hansen, P. J. Physiological and cellular adaptations of zebu cattle to thermal stress.Anim. Reprod. Sci.82-83, 349–360 (2004).

    Article CAS PubMed  Google Scholar 

  85. Matthews, R. Zebu: harbingers of doom in Bronze Age western Asia?Antiquity76, 438–446 (2002).

    Article  Google Scholar 

  86. Ollivier, M. et al. Dogs accompanied humans during the Neolithic expansion into Europe.Biol. Lett.14, 20180286 (2018).

    Article PubMed PubMed Central  Google Scholar 

  87. Ottoni, C. et al. Pig domestication and human-mediated dispersal in western Eurasia revealed through ancient DNA and geometric morphometrics.Mol. Biol. Evol.30, 824–832 (2013).

    Article CAS PubMed  Google Scholar 

  88. Ameen, C. et al. Specialized sledge dogs accompanied Inuit dispersal across the North American Arctic.Proc. R. Soc. B Biol. Sci.286, 20191929 (2019).

  89. White, S. From globalized pig breeds to capitalist pigs: a study in animal cultures and evolutionary history.Environ. Hist. Durh. N. C.16, 94–120 (2011).

    Article  Google Scholar 

  90. Bosse, M. et al. Genomic analysis reveals selection for Asian genes in European pigs following human-mediated introgression.Nat. Commun.5, 4392 (2014).

    Article CAS PubMed  Google Scholar 

  91. Bosse, M. et al. Artificial selection on introduced Asian haplotypes shaped the genetic architecture in European commercial pigs.Proc. Biol. Sci.282, 20152019 (2015).

    PubMed PubMed Central  Google Scholar 

  92. Shearin, A. L. & Ostrander, E. A. Canine morphology: hunting for genes and tracking mutations.PLoS Biol.8, e1000310 (2010).

    Article PubMed PubMed Central CAS  Google Scholar 

  93. Boyko, A. R. The domestic dog: man’s best friend in the genomic era.Genome Biol.12, 216 (2011).

    Article CAS PubMed PubMed Central  Google Scholar 

  94. Bosse, M. et al. Untangling the hybrid nature of modern pig genomes: a mosaic derived from biogeographically distinct and highly divergentSus scrofa populations.Mol. Ecol.23, 4089–4102 (2014).

    Article PubMed PubMed Central  Google Scholar 

  95. Orlando, L. & Librado, P. Origin and evolution of deleterious mutations in horses.Genes10, E649 (2019).

    Article PubMed CAS  Google Scholar 

  96. Oltenacu, P. A. & Algers, B. Selection for increased production and the welfare of dairy cows: are new breeding goals needed?Ambio34, 311–315 (2005).

    Article PubMed  Google Scholar 

  97. Charlier, C. et al. NGS-based reverse genetic screen for common embryonic lethal mutations compromising fertility in livestock.Genome Res.26, 1333–1341 (2016).

    Article CAS PubMed PubMed Central  Google Scholar 

  98. Derks, M. F. L. et al. Loss of function mutations in essential genes cause embryonic lethality in pigs.PLoS Genet.15, e1008055 (2019).

    Article CAS PubMed PubMed Central  Google Scholar 

  99. Ellegren, H. The different levels of genetic diversity in sex chromosomes and autosomes.Trends Genet.25, 278–284 (2009).

    Article CAS PubMed  Google Scholar 

  100. Peters, J., Arbuckle, B. S. & Pöllath, N. inThe Neolithic in Turkey Vol. 6 (eds Özdogan, M., Baflgelen, N. & Kuniholm, P.). 1–65 (Archaeology and Art, 2012).

  101. Wallner, B. et al. Y chromosome uncovers the recent oriental origin of modern stallions.Curr. Biol.27, 2029–2035.e5 (2017).

    Article CAS PubMed  Google Scholar 

  102. Girdland Flink, L. et al. Establishing the validity of domestication genes using DNA from ancient chickens.Proc. Natl Acad. Sci. USA111, 6184–6189 (2014).This study uses ancient DNA to show that mutations that are fixed in modern populations and that were thought to be important during chicken domestication were in fact only the target of recent artificial selection.

    Article PubMed CAS PubMed Central  Google Scholar 

  103. Loog, L. et al. Inferring allele frequency trajectories from ancient DNA indicates that selection on a chicken gene coincided with changes in medieval husbandry practices.Mol. Biol. Evol.34, 1981–1990 (2017).

    Article CAS PubMed PubMed Central  Google Scholar 

  104. Ludwig, A. et al. Coat color variation at the beginning of horse domestication.Science324, 485 (2009).

    Article CAS PubMed PubMed Central  Google Scholar 

  105. Linderholm, A. & Larson, G. The role of humans in facilitating and sustaining coat colour variation in domestic animals.Semin. Cell Dev. Biol.24, 587–593 (2013).

    Article PubMed  Google Scholar 

  106. Pavlidis, P., Jensen, J. D. & Stephan, W. Searching for footprints of positive selection in whole-genome SNP data from nonequilibrium populations.Genetics185, 907–922 (2010).

    Article CAS PubMed PubMed Central  Google Scholar 

  107. Schraiber, J. G., Evans, S. N. & Slatkin, M. Bayesian inference of natural selection from allele frequency time series.Genetics203, 493–511 (2016).

    Article CAS PubMed PubMed Central  Google Scholar 

  108. Malaspinas, A.-S. Methods to characterize selective sweeps using time serial samples: an ancient DNA perspective.Mol. Ecol.25, 24–41 (2016).

    Article CAS PubMed  Google Scholar 

  109. Barrios-Garcia, M. N. & Ballari, S. A. Impact of wild boar (Sus scrofa) in its introduced and native range: a review.Biol. Invasions14, 2283–2300 (2012).

    Article  Google Scholar 

  110. Boyd, J. M., Doney, J. M., Gunn, R. G. & Jewell, P. A. The Soay sheep of the island of Hirta, St. Kilda. A study of a feral population.Proc. Zool. Soc. London142, 129–164 (1964).

    Article  Google Scholar 

  111. Ariefiandy, A. et al. Temporal and spatial dynamics of insular Rusa deer and wild pig populations in Komodo National Park.J. Mammal.97, 1652–1662 (2016).

    Article  Google Scholar 

  112. Vigne, J.-D. et al. Pre-Neolithic wild boar management and introduction to Cyprus more than 11,400 years ago.Proc. Natl Acad. Sci. USA106, 16135–16138 (2009).

    Article CAS PubMed PubMed Central  Google Scholar 

  113. Heinsohn, T. Animal translocation: long-term human influences on the vertebrate zoogeography of Australasia (natural dispersal versus ethnophoresy).Aust. Zool.32, 351–376 (2003).

    Article  Google Scholar 

  114. Taberlet, P. et al. Are cattle, sheep, and goats endangered species?Mol. Ecol.17, 275–284 (2008).

    Article CAS PubMed  Google Scholar 

  115. Taberlet, P., Coissac, E., Pansu, J. & Pompanon, F. Conservation genetics of cattle, sheep, and goats.C. R. Biol.334, 247–254 (2011).

    Article PubMed  Google Scholar 

  116. Heckenberger, M. J., Russell, J. C., Toney, J. R. & Schmidt, M. J. The legacy of cultural landscapes in the Brazilian Amazon: implications for biodiversity.Philos. Trans. R. Soc. Lond. B Biol. Sci.362, 197–208 (2007).

    Article PubMed PubMed Central  Google Scholar 

  117. Ellis, E. C. et al. Used planet: a global history.Proc. Natl Acad. Sci. USA110, 7978–7985 (2013).

    Article CAS PubMed PubMed Central  Google Scholar 

  118. Piperno, D. R., McMichael, C. & Bush, M. B. Amazonia and the Anthropocene: what was the spatial extent and intensity of human landscape modification in the Amazon basin at the end of prehistory?Holocene25, 1588–1597 (2015).

    Article  Google Scholar 

  119. Plug, I. Aspects of life in the Kruger National Park during the early iron age.Goodwin Series6, 62–68 (1989).

    Article  Google Scholar 

  120. Spyrou, M. A., Bos, K. I., Herbig, A. & Krause, J. Ancient pathogen genomics as an emerging tool for infectious disease research.Nat. Rev. Genet.20, 323–340 (2019).

    Article CAS PubMed PubMed Central  Google Scholar 

  121. Roman-Binois, A. L’archéologie des épizooties: mise en évidence et diagnostic des crises de mortalité chez les animaux d’élevage, du Néolithique à Pasteur. (Université Panthéon-Sorbonne-Paris I, 2017).

  122. Boodhoo, N., Gurung, A., Sharif, S. & Behboudi, S. Marek’s disease in chickens: a review with focus on immunology.Vet. Res.47, 119 (2016).

    Article PubMed PubMed Central CAS  Google Scholar 

  123. Witter, R. L. The changing landscape of Marek’s disease.Avian Pathol.27, S46–S53 (1998).

    Article  Google Scholar 

  124. Bellone, R. R. et al. Evidence for a retroviral insertion in TRPM1 as the cause of congenital stationary night blindness and leopard complex spotting in the horse.PLoS One8, e78280 (2013).

    Article CAS PubMed PubMed Central  Google Scholar 

  125. FAO.Domestic animal diversity information system.DAD-IShttp://dad.fao.org/ (2017).

  126. Wood, A. R. et al. Defining the role of common variation in the genomic and biological architecture of adult human height.Nat. Genet.46, 1173–1186 (2014).

    Article CAS PubMed PubMed Central  Google Scholar 

  127. Makvandi-Nejad, S. et al. Four loci explain 83% of size variation in the horse.PLoS One7, e39929 (2012).

    Article CAS PubMed PubMed Central  Google Scholar 

  128. Racimo, F., Sankararaman, S., Nielsen, R. & Huerta-Sánchez, E. Evidence for archaic adaptive introgression in humans.Nat. Rev. Genet.16, 359–371 (2015).

    Article CAS PubMed PubMed Central  Google Scholar 

  129. Andersson, L. et al. Coordinated international action to accelerate genome-to-phenome with FAANG, the Functional Annotation of Animal Genomes Project.Genome Biol.16, 57 (2015).

    Article PubMed PubMed Central CAS  Google Scholar 

  130. Warinner, C. et al. Pathogens and host immunity in the ancient human oral cavity.Nat. Genet.46, 336–344 (2014).

    Article CAS PubMed PubMed Central  Google Scholar 

  131. Schubert, M. et al. Zonkey: a simple, accurate and sensitive pipeline to genetically identify equine F1-hybrids in archaeological assemblages.J. Archaeol. Sci.78, 147–157 (2017).

    Article  Google Scholar 

  132. Teasdale, M. D. et al. Paging through history: parchment as a reservoir of ancient DNA for next generation sequencing.Philos. Trans. R. Soc. Lond. B Biol. Sci.370, 20130379 (2015).

    Article CAS PubMed PubMed Central  Google Scholar 

  133. O’Sullivan, N. J. et al. A whole mitochondria analysis of the Tyrolean Iceman’s leather provides insights into the animal sources of Copper Age clothing.Sci. Rep.6, 31279 (2016).

    Article PubMed PubMed Central CAS  Google Scholar 

  134. Bro-Jørgensen, M. H. et al. Ancient DNA analysis of Scandinavian medieval drinking horns and the horn of the last aurochs bull.J. Archaeol. Sci.99, 47–54 (2018).

    Article  Google Scholar 

  135. Zeder, M. A. inHarlan II: Biodiversity in Agriculture: Domestication, Evolution and Sustainability (eds Damania, A. & Gepts, P.) 227–229 (Univ. California, 2011).

  136. Hanotte, O. et al. African pastoralism: genetic imprints of origins and migrations.Science296, 336–339 (2002).

    Article CAS PubMed  Google Scholar 

  137. Freeman, A. R., Bradley, D. G., Nagda, S., Gibson, J. P. & Hanotte, O. Combination of multiple microsatellite data sets to investigate genetic diversity and admixture of domestic cattle.Anim. Genet.37, 1–9 (2006).

    Article CAS PubMed  Google Scholar 

  138. Rubin, C.-J. et al. Whole-genome resequencing reveals loci under selection during chicken domestication.Nature464, 587–591 (2010).

    Article CAS PubMed  Google Scholar 

  139. Karlsson, A.-C. et al. The effect of a mutation in the thyroid stimulating hormone receptor (TSHR) on development, behaviour and TH levels in domesticated chickens.PLoS One10, e0129040 (2015).

    Article PubMed PubMed Central CAS  Google Scholar 

  140. Fang, M., Larson, G., Ribeiro, H. S., Li, N. & Andersson, L. Contrasting mode of evolution at a coat color locus in wild and domestic pigs.PLoS Genet.5, e1000341 (2009).

    Article PubMed PubMed Central CAS  Google Scholar 

  141. Andersson, L. S. et al. Mutations in DMRT3 affect locomotion in horses and spinal circuit function in mice.Nature488, 642–646 (2012).

    Article CAS PubMed PubMed Central  Google Scholar 

  142. Wutke, S. et al. The origin of ambling horses.Curr. Biol.26, R697–R699 (2016).

    Article CAS PubMed  Google Scholar 

  143. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform.Bioinformatics25, 1754–1760 (2009).

    Article CAS PubMed PubMed Central  Google Scholar 

  144. Schubert, M. et al. Improving ancient DNA read mapping against modern reference genomes.BMC Genomics13, 178 (2012).

    Article CAS PubMed PubMed Central  Google Scholar 

  145. Rajaraman, A., Tannier, E. & Chauve, C. FPSAC: fast phylogenetic scaffolding of ancient contigs.Bioinformatics29, 2987–2994 (2013).

    Article CAS PubMed  Google Scholar 

  146. Seitz, A. & Nieselt, K. Improving ancient DNA genome assembly.PeerJ5, e3126 (2017).

    Article PubMed PubMed Central CAS  Google Scholar 

  147. Patterson, N. et al. Ancient admixture in human history.Genetics192, 1065–1093 (2012).

    Article PubMed PubMed Central  Google Scholar 

  148. Patterson, N., Price, A. L. & Reich, D. Population structure and eigenanalysis.PLoS Genet.2, e190 (2006).

    Article PubMed PubMed Central CAS  Google Scholar 

  149. Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals.Genome Res.19, 1655–1664 (2009).

    Article CAS PubMed PubMed Central  Google Scholar 

  150. Durand, E. Y., Patterson, N., Reich, D. & Slatkin, M. Testing for ancient admixture between closely related populations.Mol. Biol. Evol.28, 2239–2252 (2011).

    Article CAS PubMed PubMed Central  Google Scholar 

  151. Pickrell, J. K. & Pritchard, J. K. Inference of population splits and mixtures from genome-wide allele frequency data.PLoS Genet.8, e1002967 (2012).

    Article CAS PubMed PubMed Central  Google Scholar 

Download references

Acknowledgements

L.A.F.F. and G.L. were supported by a European Research Council (ERC) grant (ERC-2013–396 StG-337574-UNDEAD) and/or Natural Environmental Research Council grants (NE/K005243/1, NE/K003259/1, NE/S00078X/1, NE/S007067/1 and NE/S007067/1). L.A.F.F. was also supported by a Wellcome Trust grant (210119/Z/18/Z). L.O. was supported by the ERC under the European Union’s Horizon 2020 research and innovation programme (grant agreement No. 681605). D.G.B. was supported by ERC Investigator grant 295729-CodeX.

Author information

Authors and Affiliations

  1. School of Biological and Chemical Sciences, Queen Mary University of London, London, UK

    Laurent A. F. Frantz

  2. Smurfit Institute of Genetics, Trinity College Dublin, Dublin, Ireland

    Daniel G. Bradley

  3. The Palaeogenomics & Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, The University of Oxford, Oxford, UK

    Greger Larson

  4. Laboratoire d’Anthropobiologie Moléculaire et d’Imagerie de Synthèse, CNRS UMR 5288, Université de Toulouse, Université Paul Sabatier, Toulouse, France

    Ludovic Orlando

  5. Lundbeck Foundation GeoGenetics Center, University of Copenhagen, Copenhagen, Denmark

    Ludovic Orlando

Authors
  1. Laurent A. F. Frantz
  2. Daniel G. Bradley
  3. Greger Larson
  4. Ludovic Orlando

Contributions

The authors contributed equally to all aspects of the article.

Corresponding authors

Correspondence toLaurent A. F. Frantz orLudovic Orlando.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information

Nature Reviews Genetics thanks S. Olsen, P. Ajmone-Marsan and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Glossary

Neolithic

An archaeological period that began ~12,000 years ago in the Near East (later in other parts of the world), following the appearance of farming communities and the domestication of plants and animals. This period marks the latest stage of the ‘Stone Age’ and ends with the development of metallurgy (Bronze Age).

Bronze Age

An archaeological period that began over 5,000 years ago in Southern Europe and part of the Near East. This period is associated with the use of bronze and, in some regions, the advent of more urban societies.

Next-generation sequencing

(NGS). Also known as ultra-high-throughput sequencing. Sequencing technologies that allow researchers to sequence entire genomes (DNA) or transcriptomes (RNA) substantially faster and cheaper than the older technologies.

Endogenous DNA

DNA extracted from the tissue (such as bone or skin) of an organism that is no longer alive, whereas exogenous DNA originates from outside (such as from soil bacteria). The proportion of endogenous DNA molecules can vary considerably depending on the origin and the age of a sample.

Capture techniques

Also known as target enrichment, these techniques help focus sequencing efforts to a subset of the DNA templates present in DNA libraries, through hybridization to target-specific probes.

Neural crest cell

A temporary cell that differentiates into multiple cell types involved in the formation of the nervous component of bones and cartilages. Research suggests that the behaviour of neural crest cells may have been modified by domestication, leading to the development of multiple traits that are common across many domesticated animal species (also known as ‘domestication syndrome’), including depigmentation, smaller brain, floppy ear and shorter muzzle.

Runs of homozygosity

(ROH). Regions of the genome that are depleted of heterozygosity, which can arise when a diploid individual inherits two identical stretches of DNA at a specific position of the genome, due to the mating of two closely related parents (such as cousins). The length and the number of ROH across the genome can provide powerful information to infer levels of inbreeding.

Artificial selection

The process by which humans breed animals to enhance specific characteristics (traits).

Yamnaya culture

An early Bronze Age culture from the northern shore of the Black Sea (Pontic steppe).

Sintashta culture

A Bronze Age culture of the northern Eurasian steppe, which is considered to be an offshoot of the Yamnaya culture.

4.2k event

A severe aridification event beginning ~4,200 years ago, which has been hypothesized to have caused the collapse of multiple civilizations across Eurasia.

Studbooks

Registries that contain the list of animals that belong to the same breed and for which the parents are known.

Breeder’s equation

A mathematical formula that allows breeders to predict the response to selection of a specific heritable trait.

Purifying selection

Also known as negative selection. Removal of deleterious variants in a population by natural selection.

Deleterious variants

Alleles that have a detrimental effect on the phenotype of an individual.

Mutational load

The mutational burden in a population or an individual resulting from deleterious variants.

Relaxed selection

The weakening or removal of a selective pressure, such as when domesticated animals are less subject to selective pressure from predators.

Justinianic plague

A historical pandemic ofYersinia pestis (541–542 ad) that affected Mediterranean port cities, including Constantinople, and that resulted in the death of 25–50 million people.

Black Death

A historical pandemic ofYersinia pestis (1346–1353 ad) that resulted in the death of 75–200 million people across Eurasia and that is thought to have had a profound effect on European history.

Rights and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Frantz, L.A.F., Bradley, D.G., Larson, G.et al. Animal domestication in the era of ancient genomics.Nat Rev Genet21, 449–460 (2020). https://doi.org/10.1038/s41576-020-0225-0

Download citation

This article is cited by

Access through your institution
Buy or subscribe

Advertisement

Search

Advanced search

Quick links

Nature Briefing

Sign up for theNature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox.Sign up for Nature Briefing

[8]ページ先頭

©2009-2025 Movatter.jp