Volume 41 Issue 1
Jan.  2020
Turn off MathJax
Article Contents
Xi-Yao Ma, Tiao Ning, Adeniyi C. Adeola, Jie Li, Ali Esmailizadeh, Jacqueline K. Lichoti, Bernard R. Agwanda, Jainagul Isakova, Almaz A. Aldashev, Shi-Fang Wu, He-Qun Liu, Najmudinov Tojiddin Abdulloevich, Manilova Elena Afanasevna, Khudoidodov Behruz Ibrohimovich, Rahamon Akinyele Moshood Adedokun, Sunday Charles Olaogun, Oscar J. Sanke, Godwin F. Mangbon, Xi Chen, Wei-Kang Yang, Zhe Wang, Min-Sheng Peng, Sheila C. Ommeh, Yan Li, Ya-Ping Zhang. Potential dual expansion of domesticated donkeys revealed by worldwide analysis on mitochondrial sequences. Zoological Research, 2020, 41(1): 51-60. doi: 10.24272/j.issn.2095-8137.2020.007
Citation: Xi-Yao Ma, Tiao Ning, Adeniyi C. Adeola, Jie Li, Ali Esmailizadeh, Jacqueline K. Lichoti, Bernard R. Agwanda, Jainagul Isakova, Almaz A. Aldashev, Shi-Fang Wu, He-Qun Liu, Najmudinov Tojiddin Abdulloevich, Manilova Elena Afanasevna, Khudoidodov Behruz Ibrohimovich, Rahamon Akinyele Moshood Adedokun, Sunday Charles Olaogun, Oscar J. Sanke, Godwin F. Mangbon, Xi Chen, Wei-Kang Yang, Zhe Wang, Min-Sheng Peng, Sheila C. Ommeh, Yan Li, Ya-Ping Zhang. Potential dual expansion of domesticated donkeys revealed by worldwide analysis on mitochondrial sequences. Zoological Research, 2020, 41(1): 51-60. doi: 10.24272/j.issn.2095-8137.2020.007

Potential dual expansion of domesticated donkeys revealed by worldwide analysis on mitochondrial sequences

doi: 10.24272/j.issn.2095-8137.2020.007
#Authors contributed equally to this work
Funds:  This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA2004010302), Second Tibetan Plateau Scientific Expedition and Research (STEP) Program (2019QZKK0501), National Natural Science Foundation of China (31860305), Sino-Africa Joint Research Center, Chinese Academy of Sciences (SAJC201611), and Research Center for Ecology and Environment of Central Asia, Chinese Academy of Sciences. Y.L. was supported by the Young Academic and Technical Leader Raising Foundation of Yunnan Province. Samples used in this study were provided by the Animal Branch of the Germplasm Bank of Wild Species, Chinese Academy of Sciences (Large Research Infrastructure Funding)
More Information
  • Molecular studies on donkey mitochondrial sequences have clearly defined two distinct maternal lineages involved in domestication. However, domestication histories of these two lineages remain enigmatic. We therefore compared several population characteristics between these two lineages based on global sampling, which included 171 sequences obtained in this study (including Middle Asian, East Asian, and African samples) plus 536 published sequences (including European, Asian, and African samples). The two lineages were clearly separated from each other based on whole mitochondrial genomes and partial non-coding displacement loop (D-loop) sequences, respectively. The Clade I lineage experienced an increase in population size more than 8 000 years ago and shows a complex haplotype network. In contrast, the population size of the Clade II lineage has remained relatively constant, with a simpler haplotype network. Although the distribution of the two lineages was almost equal across the Eurasian mainland, they still presented discernible but complex geographic bias in most parts of Africa, which are known as their domestication sites. Donkeys from sub-Saharan Africa tended to descend from the Clade I lineage, whereas the Clade II lineage was dominant along the East and North coasts of Africa. Furthermore, the migration routes inferred from diversity decay suggested different expansion across China between the two lineages. Altogether, these differences indicated non-simultaneous domestication of the two lineages, which was possibly influenced by the response of pastoralists to the desertification of the Sahara and by the social expansion and trade of ancient humans in Northeast Africa, respectively.

  • loading
  • [1]
    Andrews E. 2017. 7 Influential African Empires. From ancient Sudan to medieval Zimbabwe, get the facts on seven African kingdoms that made their mark on history. A&E Television Networks, LLC. URL: https://www.history.com/.amp/news/7-influential-african-empires.
    [2]
    Applied Biosystems. 2009. DNA Sequencing by Capillary Electrophoresis, Applied BiosystemsChemistry Guide. Thermo Fisher Scientific.
    [3]
    Bandelt HJ, Forster P, Röhl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16(1): 37−48. doi:  10.1093/oxfordjournals.molbev.a026036
    [4]
    Beja-Pereira A, England PR, Ferrand N, Jordan S, Bakhiet AO, Abdalla MA, Mashkour M, Jordana J, Taberlet P, Luikart G. 2004. African origins of the domestic donkey. Science, 304(5678): 1781. doi:  10.1126/science.1096008
    [5]
    Blench RM. 2000. A History of Donkeys, Wild Asses and Mules in Africa. London, UK: University College London Press.
    [6]
    Cardoso, J L, Vilstrup JT, Eisenmann V, Orlando L. 2013. First evidence of Equus asinus L. in the Chalcolithic disputes the Phoenicians as the first to introduce donkeys into the Iberian Peninsula. Journal of Archaeological Science, 40(12): 4483−4490. doi:  10.1016/j.jas.2013.07.010
    [7]
    Chen SY, Zhou F, Xiao H, Sha T, Wu SF, Zhang YP. 2006. Mitochondrial DNA diversity and population structure of four Chinese donkey breeds. Animal. Genetics, 37(4): 427−429. doi:  10.1111/j.1365-2052.2006.01486.x
    [8]
    Chen X, Ni G, He K, Ding ZL, Li GM, Adeola AC, Murphy RW, Wang WZ, Zhang YP. 2016. An improved de novo pipeline for enrichment of high diversity mitochondrial genomes from Amphibia to high-throughput sequencing. BioRxiv: 080689.
    [9]
    Clutton-Brock J. 1992. Horse Power: A History of the Horse and the Donkey in Human Societies. Cambridge, USA: Harvard University Press.
    [10]
    Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary. Biology, 7: 214. doi:  10.1186/1471-2148-7-214
    [11]
    Endicott P, Ho SYW, Metspalu M, Stringer C. 2009. Evaluating the mitochondrial timescale of human evolution. Trends in Ecology and Evolution, 24(9): 515−521. doi:  10.1016/j.tree.2009.04.006
    [12]
    Epstein H. 1971. The Origin of the Domestic Animals of Africa. New York, USA: African Publishing Corporation (APC).
    [13]
    Excoffier L, Lischer HEL. 2010. Arlequin suite ver3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10(3): 564−567. doi:  10.1111/j.1755-0998.2010.02847.x
    [14]
    Ge QL, Lei CZ, Jiang YQ, Chen H, Zhang W, Dang RH, Zhen HL, Zhang AL, Li TP. 2007. Genetic diversity and origins of Chinese donkey revealed by mitochondrial D-loop sequencies. Acta Veterinaria et Zootechnica Sinica, 38(7): 641−645.
    [15]
    Han L, Zhu S, Ning C, Cai D, Wang K, Chen Q, Hu S, Yang J, Shao J, Zhu H, Zhou H. 2014. Ancient DNA provides new insight into the maternal lineages and domestication of Chinese donkeys. BMC Evolutionary Biology, 14: 246. doi:  10.1186/s12862-014-0246-4
    [16]
    Herrera RJ, Garcia-Bertrand R. 2018. The Bantu Expansion. Ancestral DNA, human origins, and migrations. Academic Press, 395–432.
    [17]
    Hiernaux J. 1968. Bantu expansion: the evidence from physical anthropology confronted with linguistic and archaeological evidence. The Journal of African History, 9(4): 505−515. doi:  10.1017/S0021853700009014
    [18]
    Jordana J, Ferrando A, Miró J, Goyache F, Loarca A, Martinez López OR, Canelón JL, Stemmer A, Aguirre L, Lara MAC, Álvarez LA, Llambí S, Gómez N, Gama LT, Nóvoa MF, Martínez RD, Pérez E, Sierra A, Contreras MA, Guastella AM, Marletta D, Arsenos G, Curik I, Landi V, Martinez A, Delgado JV. 2016. Genetic relationships among American donkey populations: insights into the process of colonization. Journal of Animal Breeding and Genetics, 133(2): 155−164. doi:  10.1111/jbg.12180
    [19]
    Kefena E, Dessie T, Tegegne A, Beja-Pereira A, Yusuf Kurtu M, Rosenbom S, Han JL. 2014. Genetic diversity and matrilineal genetic signature of native Ethiopian donkeys (Equus asinus) inferred from mitochondrial DNA sequence polymorphism. Livestock Science, 167: 73−79. doi:  10.1016/j.livsci.2014.06.006
    [20]
    Kimura B, Marshall FB, Chen S, Rosenbom S, Moehlman PD, Tuross N, Sabin RC, Peters J, Barich B, Yohannes H, Kebede F, Teclai R, Beja-Pereira A, Mulligan CJ. 2011. Ancient DNA from Nubian and Somali wild ass provides insights into donkey ancestry and domestication. Proceedings of the Royal Society B: Biological Sciences, 278(1702): 50−57. doi:  10.1098/rspb.2010.0708
    [21]
    Lindsay EH, Opdyke ND, Johnson NM. 1980. Pliocene dispersal of the horse Equus and late Cenozoic mammalian dispersal events. Nature, 287: 135−138. doi:  10.1038/287135a0
    [22]
    Ma XY. 2018. Global Perspective of Phylogeography and Demongraphic History of Equus asinus Based on Mitochondrial Analysis. Master thesis, Yunnan University, China.
    [23]
    Mark JJ. 2011. Punt. Ancient History Encyclopedia. https://www.ancient.eu/punt/.
    [24]
    Marshall F. 2000. The Origins and Development of African Livestock. London: University College London Press.
    [25]
    Marshall F. 2007. Rethinking Agriculture: Archeological and Ethnoarcheological Perspectives. Walnut Creek, CA, USA: Left Coast Press.
    [26]
    Meutchieye F, Kwalar NN, Nyock RAF. 2017. Donkey Husbandry and Production Systems. Current Donkey Production and Functionality · Relationship with Humans. F. J. N. González, UCO Press.
    [27]
    Mukhtār MJa-D . 1981. Ancient Civilizations of Africa. London: Heinemann Educational Books.
    [28]
    Pérez-Pardal L, Grizelj J, Traoré A, Cubric-Curik V, Arsenos G, Dovenski T, Marković B, Fernández I, Cuervo M, Álvarez I, Beja-Pereira A, Curik I, Goyache F. 2014. Lack of mitochondrial DNA structure in Balkan donkey is consistent with a quick spread of the species after domestication. Animal Genetics, 45(1): 144−147. doi:  10.1111/age.12086
    [29]
    R-Core-Team. 2019. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. https://www.R-project.org/.
    [30]
    Rogers AR, Harpending H. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9(3): 552−569.
    [31]
    Rosenbom S, Costa V, Al-Araimi N, Kefena E, Abdel-Moneim AS, Abdalla MA, Bakhiet A, Beja-Pereira A. 2015. Genetic diversity of donkey populations from the putative centers of domestication. Animal Genetics, 46(1): 30−36. doi:  10.1111/age.12256
    [32]
    Rossel S, Marshall F, Peters J, Pilgram T, Adams MD, O'Connor D. 2008. Domestication of the donkey: timing, processes, and indicators. Proceedings of the National Academy of Sciences of the United States of America, 105(10): 3715−3720. doi:  10.1073/pnas.0709692105
    [33]
    Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A. 2017. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution, 34(12): 3299−3302. doi:  10.1093/molbev/msx248
    [34]
    Shi NN, Fan L, Yao YG, Peng MS, Zhang YP. 2014. Mitochondrial genomes of domestic animals need scrutiny. Molecular Ecology, 23(22): 5393−5397. doi:  10.1111/mec.12955
    [35]
    Smith DG, Pearson RA. 2005. A review of the factors affecting the survival of donkeys in semi-arid regions of Sub-Saharan Africa. Tropical Animal Health and Production, 37(S1): 1−19. doi:  10.1007/s11250-005-9002-5
    [36]
    South A. 2011. Rworldmap: a new R package for mapping global data. The R Journal, 3(1): 35−43. doi:  10.32614/RJ-2011-006
    [37]
    Starkey P. 2000. The History of Working Animals in Africa. London, UK: University College London Press.
    [38]
    Sun Y, Jiang Q, Yang C, Wang X, Tian F, Wang Y, Ma Y, Ju Z, Huang J, Zho X u, Zhong J, Wang C. 2016. Characterization of complete mitochondrial genome of Dezhou donkey (Equus asinus) and evolutionary analysis. Current Genetics, 62(2): 383−390. doi:  10.1007/s00294-015-0531-9
    [39]
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version6.0. Molecular Biology and Evology, 30(12): 2725−2729. doi:  10.1093/molbev/mst197
    [40]
    Thorvaldsdóttir H, Robinson JT, Mesirov JP. 2013. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Briefings Bioinformatics, 14(2): 178−192. doi:  10.1093/bib/bbs017
    [41]
    Xia X, Yu J, Zhao X, Yao Y, Zeng L, Ahmed Z, Shen S, Dang R, Lei C. 2019. Genetic diversity and maternal origin of Northeast African and South American donkey populations. Animal Genetics, 50(3): 266−270. doi:  10.1111/age.12774
    [42]
    Xie CX. 1987. The Equus Breeds in China. Shanghai: Shanghai Science & Technical Publishers. (in Chinese)
    [43]
    Xu X, Gullberg A, Arnason U. 1996. The complete mitochondrial DNA (mtDNA) of the donkey and mtDNA comparisons among four closely related mammalian species-pairs. Journal of Molecular Evolution, 43(5): 438−446. doi:  10.1007/BF02337515
  • Relative Articles

    [1] Zhe Zhang, Saber Khederzadeh, Yan Li. Deciphering the puzzles of dog domestication. Zoological Research, 2020, 41(2): 97-104.  doi: 10.24272/j.issn.2095-8137.2020.002
    [2] Xing-Han Chen, Sen Yang, Wei Yang, Yuan-Yuan Si, Rui-Wen Xu, Bin Fan, Le Wang, Zi-Ning Meng. First genetic assessment of brackish water polychaete Tylorrhynchus heterochaetus: mitochondrial COI sequences reveal strong genetic differentiation and population expansion in samples collected from southeast China and north Vietnam. Zoological Research, 2020, 41(1): 61-69.  doi: 10.24272/j.issn.2095-8137.2020.006
    [3] . Kunming Natural History Museum of Zoology. Zoological Research, 2015, 36(5): 256-.
    [4] Can LIU. Number of cranes and large waterbirds at Zhuanshanbao of Ludian County, Yunnan, China in 2013. Zoological Research, 2014, 35(S1): 227-230.  doi: 10.13918/j.issn.2095-8137.2014.s1.0227
    [5] Tshering Phuntsho, Jigme Tshering. Black-necked Crane (Grus nigricollis) in Bhutan: Current population status and conservation initiatives. Zoological Research, 2014, 35(S1): 10-19.  doi: 10.13918/j.issn.2095-8137.2014.s1.0010
    [6] Zhong-Qiu LI, Zhi WANG, Chen GE. Population trends and behavioral observations of wintering common cranes (Grus grus) in Yancheng Nature Reserve. Zoological Research, 2013, 34(5): 453-458.  doi: 10.11813/j.issn.0254-5853.2013.5.0453
    [7] LI Guo-Song, YANG Xian-Ming, ZHANG Hong-Yu, LI Wei. Population and distribution of western black crested gibbon (Nomascus concolor) at Ailao Mountain, Xinping, Yunnan. Zoological Research, 2011, 32(6): 675-683.  doi: 10.3724/SP.J.1141.2011.06675
    [8] LIU Zhi-zhi, YANG Jin-quan, WANG Zheng-qi, TANG Wen-qiao. Genetic Structure and Population History of Beleophthalmus petinirostris in Yangtze River Estuary and Its Southern Adjacent Regions. Zoological Research, 2009, 30(1): 1-10.  doi: 10.3724/SP.J.1141.2009.01001
    [9] WEI Yun-hu, ZHANG Yu-jun, CHEN Yuan, MAO Bing-yu. Expansion of the Actin Gene Family in Amphioxus. Zoological Research, 2009, 30(5): 473-479.  doi: 10.3724/SP.J.1141.2009.05473
    [10] JIANG Yan-qiong, TANG Si-xian, DING Zhi-feng, HU Hui-jian. Analysis on Color Polymorphism of Lanius schach. Zoological Research, 2008, 29(1): 99-102.
    [11] XU Feng , MA Ming , *, WU Yi-qun. Population Density and Habitat Utilization of Ibex (Capra ibex) in Tomur National Nature Reserve, Xinjiang, China(in English). Zoological Research, 2007, 28(1): 53-55.
    [12] ZHANG Yong-pu , *, DU Wei-guo, SHOU Lu. Inter-population Differences in Reproductive Life-history Traits of Blue-tailed Skinks (Eumeces elegans) from Hangzhou and Ningde, Eastern China. Zoological Research, 2006, 27(3): 255-260.
    [13] WANG Wei-wei, ZHAO Jin-liang , *, LI Si-fa. Genetic Variation of the Mitochondrial DNA Cyt b Among Six Populations of Siniperca scherzeri in China. Zoological Research, 2006, 27(6): 589-593.
    [14] NI Qing-yong MA Shi-lai , *. Population and Distribution of the Black Crested Gibbons in Southern and Southeastern Yunnan. Zoological Research, 2006, 27(1): 34-40.
    [15] LIU Bing-wan, JIANG Zhi-gang. Feces Analysis and Its Role in Wildlife Research. Zoological Research, 2002, 23(1): 71-76.
    [16] YE Shu-Feng, LU Jian-Jian. Analysis on the Spatial Distribution of Bullacta exarata (Mollusca:Gastropoda:Atyidae) Population in Yangtze River Estuary,China. Zoological Research, 2001, 22(2): 131-136.
    [17] HU Jie, HU Jin-Chu, QU Zhi-Biao, YANG Dong-Lei. Population and Age Structure of Giant Panda in Huanglongsi Nature Reserve,Sichuan,China. Zoological Research, 2000, 21(4): 287-290.
    [18] JIANG Xue-long, WANG Ying-xiang. Population and Conservation of Black-Crested Gibbons (Hylobates concolor jingdongensis) in Wuliang Nature Reserve,Jingdong,Yunnan. Zoological Research, 1999, 20(6): 421-425.
    [19] WANG Yong-jun, WAN Ben-xue, ZHOU Wei, HUANG Mu-yi. A Preliminary Investigation on the Winter Ecology of White Stork. Zoological Research, 1990, 11(4): 284-298.
    [20] MA Shi-quan. Studies on the Population Ecology of the Chinese Crowtit. Zoological Research, 1988, 9(3): 217-224.
  • ZoolRes-41-1-51-Supplementary Tables and Figures.zip
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(3)  / Tables(1)

    Article Metrics

    Article views (1223) PDF downloads(330) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return