Abstract
We investigated the genetic diversity and population genetic structure of six morphologically distinct Ethiopian donkey populations using 12 equine microsatellite markers. The donkey populations were Abyssinian (AB), Afar (AF), Hararghe (HA), Ogaden (OG), Omo (OM) and Sinnar (SI). Blood samples were collected from 180 genetically unrelated donkeys (30 individuals per population). Population genetic diversity estimates showed that total number and mean number of observed alleles, average observed and expected heterozygosity were 94, 5.208 ± 0.0229, 0.555 ± 0.023 and 0.588 ± 0.022, respectively. Highly significant deficiency in heterozygote was detected within the overall samples (FIS = 0.055 ± 0.021; P < 0.001). Though highly significant (P < 0.001), heterozygote deficiency within populations relative to total population was moderate (FST = 0.046 ± 0.016), suggesting a higher diversity within the populations (95.4%) than between populations. Various genetic distance estimation methods produced a similar topology of un-rooted dendrograms that grouped the overall Ethiopian donkeys into lowland (Ogaden, Omo and Sinnar) and highland (Abyssinian, Afar and Hararghe) genetic lineages. Likewise, Bayesian clustering analysis produced a similar pattern of clustering that was highly concordant with traditional donkey classification systems in Ethiopia.
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References
Aranguren-Mendez, J., Jordana, J., Gomez, M. 2001. Genetic diversity in Spanish donkey breeds using microsatellite DNA markers. Genetics Selection Evolution, 33, 433-442
Beja-Pereira, A., England, P.R., Ferrand, N., Jordan, S., Bakhiet, A.O., Abdalla, M.A., Mashkour, M., Jordana, J., Taberlet, P., Luikart, G. 2004. African origin of domestic donkey. Science, 304, 1781.
Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., Bonhomme, F. 2001. GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier, France.
Blench, R.M., 2000. A history of donkeys, wild asses and mules in Africa. In: Blench, R. M., MacDonald, K. C. (eds.), The origin and development of African livestock: archaeology, genetics, linguistics and ethnography. UCL Press, pp: 339–354.
Bren M., Downs P., Irvin Z., Bell K. 1994a. Intrageneric amplification of horse microsatellite markes with emphasis on the Przewalski’s horse (E. przewalski). Animal Genetics, 25, 401-405.
Bren, M., Downs, P., Irvin, Z., Bell, K. 1994b. Six equine dinuleotide repeats: microsatellites MPZ002, 3, 4, 5, 6 and 7. Animal Genetics, 25, 124.
Earl, D.A., vonHoldt, B.M. 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359-361.
Evanno, G., Regnau, T S., Goudet, J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Evolution, 14, 2611-2620.
Felsenstein, J. 1989–2006. PHYLIP (phylogeny inference package). Version 3.66. Seattle (WA): Genomes Sciences, Department of Genetics. University of Washington Software available from http://evolution.genetics.washington.edu/phylip.html.
Guo, S.W., Thompson, E.A. 1992. Performing the exact test of Hardy–Weinberg proportions for multiple alleles. Biometrics, 48, 361-372.
Ishida, N., Oyunsuren, T., Mashima, S., Mukoyama, H., Saitou N. 1995. Mitochondrial DNA sequences of various species of the genus Equus with special reference to the phylogenetic relationship between Przewalskii’s wild horse and domestic horse. Journal of Molecular Evolution, 41, 180-188.
Ivankovic, A., Kavar, T., Caput, P., Mioc, B., Pavic, V., Dovc, P. 2002. Genetic diversity of three donkey populations in the Croatian costal region. Animal Genetics, 33, 169-177.
Jakobsson, M., Rosenberg, N.A. 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23, 1801-1806.
Jordana, J., Folch, P., Aranguren, J.A. 2001. Microsatellite analysis of genetic diversity in the Catalonian donkey breed. Journal of Animal Breeding and Genetics, 118, 57-63
Kefena, E., Beja-Pereira, A., Han, J.L., Haile, A., Mohammed, Y.K., Dessie, T. 2011. Eco-geographical structuring and morphological diversities in Ethiopian donkey populations. Livestock Science, 141, 232-241.
Kefena, E., Rosenbom, S., Han, J., Dessie, T., Beja-Pereira, B. 2021. Genetic diversities and historical dynamics of native Ethiopian horse populations (Equus caballus) inferred from mitochondrial DNA polymorphisms. Genes, 12, 155.
Kimura, B., Marshall, F., Chen, S., Rosenbom, S., Moehlman, P.D., Tuross, N., Sabin, R.C., Peters, J., Barich, B., Yohannes, H., Kebede, F., Teclai, R., Beja-Pereira, A., Mulligan, C.J. 2011. Ancient DNA from Nubian and Somali wild ass provides insights into donkey ancestry and domestication. Proceeding of the Royal Society of Biological Sciences, 278, 50-57.
Langella, O. 1999. Populations version 1.2.30. Available at: http://bioinformatics.org/~tryphon/populations/.
Lei, C.Z., Ge, Q. L., Zhang, H.C., Liu, R.Y., Zhang, W., Jiang, Y.Q., Dang, R.H., Zheng, H.L., Hou, W.T., Chen, H. 2007. African maternal origin and genetic diversity of Chinese domestic donkeys. Asian-Australian Journal of Animal Sciences, 20(5), 645-652.
Lopez Lopez, C., Alonso, R., de Aluja, A.S. 2005. Study of the genetic origin of the Mexican Creole donkey (Equus asinus) by means of the analysis of the D-loop region of mitochondrial DNA. Tropical Animal Health and Production, 37, 173-188.
Luikart, G., Allendorf, F.W., Cornuet, J.M., Sherwin, W.B. 1998. Distortion of allele frequency distributions provides a test for recent population bottlenecks. Journal of Heredity, 89, 238-247.
Marshall, F. 2007. African pastoral perspectives on domestication of the donkey: A first synthesis. In: Denham, T.P., Jriarte, J., Vrydaghs, L. (eds.), Rethinking agriculture: archaeological and ethno archaeological perspectives, One World Archaeology Series, Walnut Creek, CA, Left Coast Press. pp: 371-407.
Moehlman, P.D. 2002. Status and action plan for the African wild ass. In: Moehlman, P.D. (eds.), Equids: Zebras, Asses and Horses, Status Survey and Conservation Action Plan, IUCN, Gland, Switzerland. pp: 2-9.
Nei, M. 1987. Molecular Evolutionary Genetics. Columbia University Press, New York, USA.
Nei, M., Tajima, F., Tateno Y. 1983. Accuracy of estimated phylogenetic trees from molecular data. Journal of Molecular Evolution, 19, 153-170.
Page, R.D.M. 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Compendium of Applied Biosciences, 12, 357-358.
Peakall, R., Smouse, P.E. 2006. GENALEX 6.41: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6: 288-295.
Pritchard, J.K., Stephens, M., Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
Raymond, M., Rousset, F. 1995. GENEPOP (version 3.3): Population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248-249.
Reynolds, J., Weir, B.S., Cokerham, C. 1983. Estimation of the co-ancestry coefficients: basis for a short-term genetic distance. Genetics, 105,767-79.
Rosenberg, N.A. 2004. DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes, 4, 137-138.
Rosenbom, R., Costa, V., Al-Araimi, N., Kefena, E., Abdel-Moneim, A.S., Abdalla, M.A., Bakhiet, A., Beja-Pereira, A. 2014. Genetic diversity of donkey populations from the putative centers of domestication. Animal Genetics, 46, 30-36.
Rossel, S., Marshall, F., Peters, J., Pilgram, T., Adams, M.D., O’Connor, D. 2008. Domestication of the donkey: timing, processes and indicators. Proceedings of the National Academy of Sciences, 105, 3715-3720.
Saitou, N., Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Ecology and Evolution, 4, 406-425.
Watson, M. 1982. Draft report on the African wild ass. Arusha, Tanzania. 5pp.
Weir, B.S., Cockerham, C.C. 1984. Estimation of F-statistics for the analysis of population structure. Evolution, 38, 1358-1370.
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, 438-446.
Funding
This work is part of a Ph.D. project granted to the first author by the German Academic Exchange Services (DAAD) in collaboration with the International Livestock Research Institute (ILRI) in their regional program. It was also partially supported by the Portuguese Foundation for Science (FCT) through the project PTDC/BIA-BDE/64111/2006.
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Effa Kefena (Ph.D.): conceived and designed the study, performed the research, analyzed the data and prepared the draft manuscript.
S. Rosenbom (Ph.D.): assisted and performed lab analysis
A. Beja-Pereira (Prof.): hosted the first author at his lab, provided logistic and funding support and edited the manuscript before submission.
J. L. Han (Prof.): provided kits for field sample collections, supported in data analysis and edited the final manuscript before submission.
M. Yusuf Kurtu (Prof.): hosted the first author at Haramaya University and facilitated logistic supports during field data collection.
T. Dessie (Ph.D.): hosted the first author at the International Livestock Research Institute (ILRI) as a PhD student, facilitated logistic supports during field data collection.
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All ethical standards for the phenotypic characterization of farm animal genetic resources have been strictly followed and applied.
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The study has been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments as well as following a guideline “Phenotypic Characterization of Animal Genetic Resources” (2012) developed by Food and Agricultural Organization of the United Nations.
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Supplementary Information
ESM 1
Supporting Figure S1 Un-rooted neighbor-joining dendrogram summarizing the genetic relationships between six donkey populations of Ethiopia. (PNG 205 kb)
ESM 3
Supporting Figure S3 Genetic structure and individual membership of Ethiopian donkeys (K = 2 to 6). (PNG 81 kb)
ESM 4
Supporting Figure S4 Genetic structure and population membership of Ethiopian donkeys (K = 2 to 6). (JPG 366 kb)
ESM 5
Supporting Table S1 Modified laboratory protocol used to extract nuclear DNA from Whatman FTA Classic Cards. (DOC 68 kb)
ESM 6
Supporting Table S2 Oligonucleotide sequence, fluorescent label and annealing temperature of 12 microsatellites used in this study. (DOC 33 kb)
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Supporting Table S3 P-values of Hardy-Weinberg equilibrium tests. (DOC 40 kb)
ESM 8
Supporting Table S4 Estimates of within-population inbreeding co-efficient (FIS) for each locus and overall loci in six Ethiopian donkey populations. (DOC 104 kb)
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Kefena, E., Rosenbom, S., Beja-Pereira, A. et al. Genetic diversity and population genetic structure in native Ethiopian donkeys (Equus asinus) inferred from equine microsatellite markers. Trop Anim Health Prod 53, 334 (2021). https://doi.org/10.1007/s11250-021-02776-2
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DOI: https://doi.org/10.1007/s11250-021-02776-2
Keywords
- Ethiopian donkey
- Genetic diversity
- Geographic clustering; Microsatellite marker