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Research on Prehistoric Genomes Reveal the Cost of Equine Domestication

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The Proceedings of the National Academy of Sciences of the United States of America (PNAS.org) has made available the abstract titled “Prehistoric genomes reveal the genetic foundation and cost of horse domestication.” The researchers note that, “we show that modern horse genomes contain an excess of deleterious mutations, likely representing the genetic cost of domestication.”

Significance

“The domestication of the horse revolutionized warfare, trade, and the exchange of people and ideas. This at least 5,500-y-long process, which ultimately transformed wild horses into the hundreds of breeds living today, is difficult to reconstruct from archeological data and modern genetics alone. We therefore sequenced two complete horse genomes, predating domestication by thousands of years, to characterize the genetic footprint of domestication. These ancient genomes reveal predomestic population structure and a significant fraction of genetic variation shared with the domestic breeds but absent from Przewalski’s horses. We find positive selection on genes involved in various aspects of locomotion, physiology, and cognition. Finally, we show that modern horse genomes contain an excess of deleterious mutations, likely representing the genetic cost of domestication.”

Abstract

“The domestication of the horse ∼5.5 kya and the emergence of mounted riding, chariotry, and cavalry dramatically transformed human civilization. However, the genetics underlying horse domestication are difficult to reconstruct, given the near extinction of wild horses. We therefore sequenced two ancient horse genomes from Taymyr, Russia (at 7.4- and 24.3-fold coverage), both predating the earliest archeological evidence of domestication. We compared these genomes with genomes of domesticated horses and the wild Przewalski’s horse and found genetic structure within Eurasia in the Late Pleistocene, with the ancient population contributing significantly to the genetic variation of domesticated breeds. We furthermore identified a conservative set of 125 potential domestication targets using four complementary scans for genes that have undergone positive selection. One group of genes is involved in muscular and limb development, articular junctions, and the cardiac system, and may represent physiological adaptations to human utilization. A second group consists of genes with cognitive functions, including social behavior, learning capabilities, fear response, and agreeableness, which may have been key for taming horses. We also found that domestication is associated with inbreeding and an excess of deleterious mutations. This genetic load is in line with the “cost of domestication” hypothesis also reported for rice, tomatoes, and dogs, and it is generally attributed to the relaxation of purifying selection resulting from the strong demographic bottlenecks accompanying domestication. Our work demonstrates the power of ancient genomes to reconstruct the complex genetic changes that transformed wild animals into their domesticated forms, and the population context in which this process took place."

Authors

1. Mikkel Schuberta,1,

2. Hákon Jónssona,1,

3. Dan Changb,1,

4. Clio Der Sarkissiana,

5. Luca Erminia,

6. Aurélien Ginolhaca,

7. Anders Albrechtsenc,

8. Isabelle Dupanloupd,e,

9. Adrien Foucald,e,

10. Bent Petersenf,

11. Matteo Fumagallig,

12. Maanasa Raghavana,

13. Andaine Seguin-Orlandoa,h,

14. Thorfinn S. Korneliussena,

15. Amhed M. V. Velazqueza,

16. Jesper Stenderupa,

17. Cindi A. Hooveri,

18. Carl-Johan Rubinj,

19. Ahmed H. Alfarhank,

20. Saleh A. Alquraishik,

21. Khaled A. S. Al-Rasheidk,

22. David E. MacHughl,m,

23. Ted Kalbfleischn,

24. James N. MacLeodo,

25. Edward M. Rubini,

26. Thomas Sicheritz-Pontenf,

27. Leif Anderssonj,

28. Michael Hofreiterp,

29. Tomas Marques-Bonetq,r,

30. M. Thomas P. Gilberta,

31. Rasmus Nielsens,

32. Laurent Excoffierd,e,

33. Eske Willersleva,

34. Beth Shapirob,

35. Ludovic Orlandoa,2

1. aCentre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350K Copenhagen, Denmark;

2. bDepartment of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064;

3. cThe Bioinformatics Centre, Department of Biology, University of Copenhagen, 2200N Copenhagen, Denmark;

4. dInstitute of Ecology and Evolution, University of Berne, 3012 Berne, Switzerland;

5. eSwiss Institute of Bioinformatics, 1015 Lausanne, Switzerland;

6. fCenter for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark, 2800 Lyngby, Denmark;

7. gUCL Genetics Institute, Department of Genetics, Evolution, and Environment, University College London, London WC1E 6BT, United Kingdom;

8. hNational High-Throughput DNA Sequencing Center, University of Copenhagen, 1353K Copenhagen, Denmark;

9. iDepartment of Energy Joint Genome Institute, Walnut Creek, CA 94598;

10. jScience for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, SE-751 23 Uppsala, Sweden;

11. kZoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia;

12. lAnimal Genomics Laboratory, UCD School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland;

13. mUCD Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Dublin 4, Ireland;

14. nBiochemistry and Molecular Biology, School of Medicine, University of Louisville, Louisville, KY 40292;

15. oDepartment of Veterinary Science, Gluck Equine Research Center, University of Kentucky, Lexington, KY 40546;

16. pInstitute for Biochemistry and Biology, Faculty for Mathematics and Natural Sciences, University of Potsdam, 14476 Potsdam, Germany;

17. qInstituticó Catalana de Recerca i Estudis Avançats, Institut de Biologia Evolutiva (Universitat Pompeu Fabra/Consejo Superior de Investigaciones Cientificas), 08003 Barcelona, Spain;

18. rCentro Nacional de Análisis Genómico, 08028 Barcelona, Spain; and

19. sDepartments of Integrative Biology and Statistics, University of California, Berkeley, CA 94720

The Proceedings was edited by David M. Hillis, The University of Texas at Austin, Austin, TX, and approved November 13, 2014 (received for review September 4, 2014).