Mitochondrial Sequence Variation, Haplotype Diversity, and Relationships Among Dromedary Camel-Types

Randa Alaqeely 1, Bader H Alhajeri 1, Faisal Almathen 2 3, Hasan Alhaddad 1

Affiliations

30 August 2021

-

doi: 10.3389/fgene.2021.723964

Abstract

Dromedary camels are outstanding livestock that developed efficient abilities to tolerate desert conditions. Many dromedary camel-types (i.e., named populations) exist but lack defined specific breed standards, registries, and breeders' governing organizations. The breed status of dromedary camel-types can partly be assessed by exploring mitochondrial DNA (mtDNA) variation. Accordingly, this study aimed to examine the breed status and the inter-population relationships of dromedary camel-types by analyzing sequence variation in the mtDNA control region and in three coding genes [cytochrome b, threonine, and proline tRNA, and part of the displacement loop (D-loop)] (867 bp region). Tail hair samples (n = 119) that represent six camel-types from Kuwait were collected, extracted, sequenced, and compared to other publicly available sequences (n = 853). Within the sequenced mitochondrial region, 48 polymorphic sites were identified that contributed to 82 unique haplotypes across 37 camel-types. Haplotype names and identities were updated to avoid previous discrepancies. When all sequences were combined (n = 972), a nucleotide diversity of 0.0026 and a haplotype diversity of 0.725 was observed across the dromedary-types. Two major haplogroups (A and B) were identified and the B1 haplotype was predominant and found in almost all dromedary-types whereas the A haplotypes were more abundant in African regions. Non-metric multidimensional scaling revealed an increased similarity among Arabian Peninsula "Mezayen" camel-types, despite their defining coat colors. The relationships among dromedary camel-types can partly be explained by mtDNA. Future work aimed at a deeper understanding of camel-type breed status should focus on a high number of nuclear markers.

Keywords: camel; haplogroup; mtDNA; polymorphism; population.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1 A graphical representation of the sequenced mtDNA fragment along with the parsimony informative sites and their minor allele frequency. Vertical lines represent the minor allele frequencies (MAF) of parsimony informative sites. Singletons were excluded.

FIGURE 1 A graphical representation of the sequenced mtDNA fragment along with the parsimony informative sites and their minor allele frequency. Vertical lines represent the minor allele frequencies (MAF) of parsimony informative sites. Singletons were excluded.

FIGURE 2 Unrooted phylogenetic tree of the 82 dromedary camel haplotypes. The new haplotype naming system based on this study. Values above branches are posterior probabilities (PP). Blue branch lines indicate haplogroup B sequences with posterior probability values = 1, while the yellow line designate haplogroup A sequences with a posterior probability = 1. Branches colored in black have PP values < 1.

FIGURE 2 Unrooted phylogenetic tree of the 82 dromedary camel haplotypes. The new haplotype naming system based on this study. Values above branches are posterior probabilities (PP). Blue branch lines indicate haplogroup B sequences with posterior probability values = 1, while the yellow line designate haplogroup A sequences with a posterior probability = 1. Branches colored in black have PP values < 1.

FIGURE 3 Median Joining Network of 867 bp camel mtDNA sequences. Singletons were excluded resulting in 47 haplotypes. Red circles represent median vectors. Colors are based on haplotype identity and frequency.

FIGURE 3 Median Joining Network of 867 bp camel mtDNA sequences. Singletons were excluded resulting in 47 haplotypes. Red circles represent median vectors. Colors are based on haplotype identity and frequency.

FIGURE 4 Frequencies of haplotypes of different camel-types grouped according to their naming criteria. Camel-types represented by <5 individuals were not plotted. Camel-types with unknown naming system are not shown.

FIGURE 4 Frequencies of haplotypes of different camel-types grouped according to their naming criteria. Camel-types represented by <5 individuals were not plotted. Camel-types with unknown naming system are not shown.

FIGURE 5 Non-metric multidimensional scaling plot constructed using the Fst values between each pair of the 30 camel-types. (A) All camel-types. (B) Expanded view of the camel-types enclosed in the dashed box in panel (A). Each dot represents a camel-type.

FIGURE 5 Non-metric multidimensional scaling plot constructed using the Fst values between each pair of the 30 camel-types. (A) All camel-types. (B) Expanded view of the camel-types enclosed in the dashed box in panel (A). Each dot represents a camel-type.

FIGURE 6 Unrooted phylogenetic tree of Mezayen camel-type haplotypes. Values above branches correspond to the posterior probability values. Posterior probability values = 1 were omitted for clarity. The dashed box contains haplotype A sequences. Non-major (low frequency) B haplotypes were illustrated at the tip of the branches. Photos are taken by HA.

FIGURE 6 Unrooted phylogenetic tree of Mezayen camel-type haplotypes. Values above branches correspond to the posterior probability values. Posterior probability values = 1 were omitted for clarity. The dashed box contains haplotype A sequences. Non-major (low frequency) B haplotypes were illustrated at the tip of the branches. Photos are taken by HA.

Similar articles

Genetic Diversity and Population Structure of Dromedary Camel-Types.

AlAskar H, Alhajeri BH, Almathen F, Alhaddad H.J Hered. 2020 Aug 12;111(4):405-413. doi: 10.1093/jhered/esaa016.PMID: 32530038

Mitochondrial DNA variation and phylogeography of Old World camels.

Ming L, Siren D, Yi L, Hai L, He J, Ji R.Anim Biosci. 2021 Apr;34(4):525-532. doi: 10.5713/ajas.20.0319. Epub 2020 Aug 24.PMID: 32898955 Free PMC article.

Homogeneity of Arabian Peninsula dromedary camel populations with signals of geographic distinction based on whole genome sequence data.

Bahbahani H, Almathen F.Sci Rep. 2022 Jan 7;12(1):130. doi: 10.1038/s41598-021-04087-w.PMID: 34997084 Free PMC article.

Aspects of Molecular Genetics in Dromedary Camel.

Piro M.Front Genet. 2021 Oct 21;12:723181. doi: 10.3389/fgene.2021.723181. eCollection 2021.PMID: 34764978 Free PMC article. Review.

Coxiella burnetii in Dromedary Camels (Camelus dromedarius): A Possible Threat for Humans and Livestock in North Africa and the Near and Middle East?

Devaux CA, Osman IO, Million M, Raoult D.Front Vet Sci. 2020 Nov 5;7:558481. doi: 10.3389/fvets.2020.558481. eCollection 2020.PMID: 33251255 Free PMC article. Review.

Cited by

Exploiting morphobiometric and genomic variability of African indigenous camel populations-A review.

Yakubu A, Okpeku M, Shoyombo AJ, Onasanya GO, Dahloum L, Çelik S, Oladepo A.Front Genet. 2022 Dec 12;13:1021685. doi: 10.3389/fgene.2022.1021685. eCollection 2022.PMID: 36579332 Free PMC article.

Genetic similarity and diversity among three camel populations reared in Egypt.

Abdel-Aziem SH, Mabrouk DM, Abd El-Kader HA, Alam SS, Othman OE.J Genet Eng Biotechnol. 2022 Nov 3;20(1):154. doi: 10.1186/s43141-022-00435-z.PMID: 36326964 Free PMC article.

KMEL References

https://pubmed.ncbi.nlm.nih.gov/

References

  1.  
    1. Abdallah H., Faye B. (2013). Typology of camel farming system in Saudi Arabia. Emirates J. Food Agric. 25 250–260.
  2.  
    1. Abdallah H. R., Faye B. (2012). Phenotypic classification of Saudi Arabian camel (Camelus dromedarius) by their body measurements. Emirates J. Food Agric. 24 272–280.
  3.  
    1. Abdussamad A. M., Charruau P., Kalla D. J. U., Burger P. A. (2015). Validating local knowledge on camels: colour phenotypes and genetic variation of dromedaries in the Nigeria-Niger corridor. Livestock Sci. 181 131–136. 10.1016/j.livsci.2015.07.008 - DOI
  4.  
    1. Achaaban M. R., Mouloud M., Tligui N. S., El Allali K. (2016). Main anatomical and histological features of the tonsils in the camel (Camelus dromedarius). Trop. Anim. Health Prod. 48 1653–1659. 10.1007/s11250-016-1139-x - DOI - PubMed
  5.  
    1. Adamsons K., Jr., Engel S. L., Van Dyke H. B., Schmidt-Nielsen B., Schmidt-Nielsen K. (1956). The distribution of oxytocin and vasopressin (antidiuretic hormone) in the neuro-hypophysis of the camel. Endocrinology 58 272–278. 10.1210/endo-58-2-272 - DOI - PubMed
  6.  
    1. Ahmed S., Grobler P., Madisha T., Kotze A. (2016). Mitochondrial D-loop sequences reveal a mixture of endemism and immigration in Egyptian goat populations. Mitochond. DNA Part A 28 711–716. 10.3109/24701394.2016.1174225 - DOI - PubMed
  7.  
    1. Akaike H. (1974). A new look at the statistical model identification. IEEE Trans. Automatic Control 19 716–723.
  8.  
    1. AlAskar H., Alhajeri B. H., Almathen F., Alhaddad H. (2020). Genetic diversity and population structure of dromedary camel-types. J. Hered. 111 405–413. 10.1093/jhered/esaa016 - DOI - PubMed
  9.  
    1. Alaskar H. M., Alaqeely R., Alhajeri B. H., Alhaddad H. (2021). The enigma of camel-types: localities, utilities, names, and breed statuses. J. Camelid Sci. 14 22–34.
  10.  
    1. Alhaddad H., Alhajeri B. H. (2018). SamplEase: a simple application for collection and organization of biological specimen data in the field. Ecol. Evol. 8 10266–10271. 10.1002/ece3.4503 - DOI - PMC - PubMed
  11.  
    1. Alhaddad H., Alhajeri B. H. (2019). Cdrom archive: a gateway to study camel phenotypes. Front. Genet. 10:48. 10.3389/fgene.2019.00048 - DOI - PMC - PubMed
  12.  
    1. Alhaddad H., Maraqa T., Alabdulghafour S., Alaskar H., Alaqeely R., Almathen F., et al. (2019). Quality and quantity of dromedary camel DNA sampled from whole-blood, saliva, and tail-hair. PLoS One 14:e0211743. 10.1371/journal.pone.0211743 - DOI - PMC - PubMed
  13.  
    1. Alhajeri B. H., Alaqeely R., Alhaddad H. (2019). Classifying camel breeds using geometric morphometrics: a case study in Kuwait. Livestock Sci. 230:103824. 10.1016/j.livsci.2019.103824 - DOI
  14.  
    1. Al-Hazmi M., Ghandour A., ElGohar M. (1994). A study of the biometry of some breeds of arabian camel (camelus dromedarius) in Saudi Arabia. Science 6 87–99.
  15.  
    1. Almathen F., Charruau P., Mohandesan E., Mwacharo J. M., Orozco-terWengel P., Pitt D., et al. (2016). Ancient and modern DNA reveal dynamics of domestication and cross-continental dispersal of the dromedary. Proc. Natl. Acad. Sci. U.S.A. 113 6707–6712. 10.1073/pnas.1519508113 - DOI - PMC - PubMed
  16.  
    1. Alsafy M., El-Gendy S., El Sharaby A. (2013). Anatomic reference for computed tomography of paranasal sinuses and their communication in the Egyptian buffalo (Bubalus bubalis). Anat. Histol. Embryol. 42 220–231. 10.1111/ahe.12005 - DOI - PubMed
  17.  
    1. Arman K. (2007). A new direction for kennel club regulations and breed standards. Can. Vet. J. 48 953–965. - PMC - PubMed
  18.  
    1. Atig R. K., Hsouna S., Beraud-Colomb E., Abdelhak S. (2009). Mitochondrial DNA: properties and applications. Arch. Inst. Pasteur Tunis 86 3–14. - PubMed
  19.  
    1. Bandelt H.-J., Forster P., Röhl A. (1999). Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16 37–48. - PubMed
  20.  
    1. Casey C. S., Orozco-terWengel P., Yaya K., Kadwell M., Fernández M., Marín J. C., et al. (2018). Comparing genetic diversity and demographic history in co-distributed wild South American camelids. Heredity 121 387–400. 10.1038/s41437-018-0120-z - DOI - PMC - PubMed
  21.  
    1. Cieslak M., Pruvost M., Benecke N., Hofreiter M., Morales A., Reissmann M., et al. (2010). Origin and history of mitochondrial DNA lineages in domestic horses. PLoS One 5:e15311. 10.1371/journal.pone.0015311 - DOI - PMC - PubMed
  22.  
    1. Cozzi M. C., Valiati P., Cherchi R., Gorla E., Prinsen R. T. M. M., Longeri M., et al. (2018). Mitochondrial DNA genetic diversity in six Italian donkey breeds (Equus asinus). Mitochondr. DNA Part A 29 409–418. - PubMed
  23.  
    1. Di Lorenzo P., Ceccobelli S., Panella F., Attard G., Lasagna E. (2015). The role of mitochondrial DNA to determine the origin of domestic chicken. World’s Poult. Sci. J. 71 311–318.
  24.  
    1. Di Lorenzo P., Lancioni H., Ceccobelli S., Colli L., Cardinali I., Karsli T., et al. (2018). Mitochondrial DNA variants of Podolian cattle breeds testify for a dual maternal origin. PLoS One 13:e0192567. 10.1371/journal.pone.0192567 - DOI - PMC - PubMed
  25.  
    1. Djazouli Alim F. Z., Rodriguez M. J., Andrade C., Lebaili N., Mahy N. (2012). Adaptation of Camelus dromedarius pars nervosa of the hypophysis to winter and summer living conditions. Folia Histochem. Cytobiol. 50 203–212. 10.5603/FHC.2012.002 - DOI - PubMed
  26.  
    1. Doosti A., Dehkordi P. G. (2011). Genetic polymorphisms of mitochondrial genome D-loop region in Bakhtiarian population by PCR-RFLP. Int. J. Biol. 3:41.
  27.  
    1. Excoffier L., Lischer H. E. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resourc. 10 564–567. - PubMed
  28.  
    1. FAO (2013). In Vivo Conservation of Animal Genetic Resources. Rome: Food and Agriculture Organization of the United Nations.
  29.  
    1. FAO (2017). Food and Agricultural Organization, United Nations. [Online]. Available online at: http://www.fao.org/faostat/en/#data (accessed on 2018)
  30.  
    1. González B. A., Vásquez J. P., Gómez-Uchida D., Cortés J., Rivera R., Aravena N., et al. (2019). Phylogeography and population genetics of Vicugna vicugna: evolution in the arid andean high plateau. Front. Genet. 10:445. 10.3389/fgene.2019.00445 - DOI - PMC - PubMed
  31.  
    1. Hall T. (2013). BioEdit, Version 7.2. 5. Carlsbad, CA: Ibis Biosciences.
  32.  
    1. Hasegawa M., Kishino H., Yano T.-A. (1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22 160–174. 10.1007/bf02101694 - DOI - PubMed
  33.  
    1. Hristov P., Yordanov G., Ivanova A., Mitkov I., Sirakova D., Mehandzyiski I., et al. (2017). Mitochondrial diversity in mountain horse population from the South-Eastern Europe. Mitochondr. DNA Part A 28 787–792. 10.1080/24701394.2016.1186667 - DOI - PubMed
  34.  
    1. Huelsenbeck J. P., Ronquist F. (2001). MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17 754–755. 10.1093/bioinformatics/17.8.754 - DOI - PubMed
  35.  
    1. Hutchison C. A., III, Newbold J. E., Potter S. S., Edgell M. H. (1974). Maternal inheritance of mammalian mitochondrial DNA. Nature 251 536. 10.1038/251536a0 - DOI - PubMed
  36.  
    1. Ishag I., Reissmann M., Peters K., Musa L., Ahmed M. (2010). Phenotypic and molecular characterization of six Sudanese camel breeds. South Afr. J. Anim. Sci. 40 319–326.
  37.  
    1. Jansen T., Forster P., Levine M. A., Oelke H., Hurles M., Renfrew C., et al. (2002). Mitochondrial DNA and the origins of the domestic horse. Proc. Natl. Acad. Sci. U.S.A. 99 10905. 10.1073/pnas.152330099 - DOI - PMC - PubMed
  38.  
    1. Jukes T. H. (1987). Transitions, transversions, and the molecular evolutionary clock. J. Mol. Evol. 26 87–98. - PubMed
  39.  
    1. Kadwell M., Fernandez M., Stanley H. F., Baldi R., Wheeler J. C., Rosadio R., et al. (2001). Genetic analysis reveals the wild ancestors of the llama and the alpaca. Proc. R. Soc. Lond. Ser. B Biol. Sci. 268 2575–2584. - PMC - PubMed
  40.  
    1. Kavar T., Habe F., Brem G., Dovč P. (1999). Mitochondrial D-loop sequence variation among the 16 maternal lines of the Lipizzan horse breed. Anim. Genet. 30 423–430. 10.1046/j.1365-2052.1999.00557.x - DOI - PubMed
  41.  
    1. Kawabe K., Worawut R., Taura S., Shimogiri T., Nishida T., Okamoto S. (2014). Genetic diversity of mtDNA D-loop polymorphisms in laotian native fowl populations. Asian Austr. J. Anim. Sci. 27 19–23. 10.5713/ajas.2013.13443 - DOI - PMC - PubMed
  42.  
    1. Kibegwa F., Githui K., Jung’a J., Badamana M., Nyamu M. (2016). Mitochondrial DNA variation of indigenous goats in Narok and Isiolo counties of Kenya. J. Anim. Breed. Genet. 133 238–247. - PubMed
  43.  
    1. Kimura B., Marshall F. B., Chen S., Rosenbom S., Moehlman P. D., Tuross N., et al. (2010). Ancient DNA from Nubian and Somali wild ass provides insights into donkey ancestry and domestication. Proc. R. Soc. B Biol. Sci. 278 50–57. - PMC - PubMed
  44.  
    1. Kumar S., Stecher G., Li M., Knyaz C., Tamura K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35 1547–1549. 10.1093/molbev/msy096 - DOI - PMC - PubMed
  45.  
    1. Leese A. S. (1927). A Treatise on the One-Humped Camel in Health and in Disease. Stanford: Haines.
  46.  
    1. Legesse Y. W., Dunn C. D., Mauldin M. R., Ordonez-Garza N., Rowden G. R., Gebre Y. M., et al. (2018). Morphometric and genetic variation in 8 breeds of Ethiopian camels (Camelus dromedarius). J. Anim. Sci. 96 4925–4934. 10.1093/jas/sky351 - DOI - PMC - PubMed
  47.  
    1. Lynghaug F. (2009). The Official Horse Breeds Standards Guide: The Complete Guide to the Standards of All North American Equine Breed Associatio. Minneapolis, MN: Voyageur Press.
  48.  
    1. Mahmoud A. H., Abu-Tarbush F. M., Alshaik M., Aljumaah R., Saleh A. (2019). Genetic diversity and population genetic structure of six dromedary camel (camelus dromedarius) populations in Saudi Arabia. Saudi J. Biol. Sci. 27 1384–1389. 10.1016/j.sjbs.2019.11.041 - DOI - PMC - PubMed
  49.  
    1. Mahrous K. F., Ramadan H., Abdel-Aziem S. H., Abd-El Mordy M., Hemdan D. M. (2011). Genetic variations between camel breeds using microsatellite markers and RAPD techniques. J. Appl. Biosci. 39 2626–2634.
  50.  
    1. Mburu D., Ochieng J., Kuria S., Jianlin H., Kaufmann B., Rege J., et al. (2003). Genetic diversity and relationships of indigenous Kenyan camel (Camelus dromedarius) populations: implications for their classification. Anim. Genet. 34 26–32. 10.1046/j.1365-2052.2003.00937.x - DOI - PubMed
  51.  
    1. McMillan W. O., Palumbi S. R. (1997). Rapid rate of control-region evolution in Pacific butterflyfishes (Chaetodontidae). J. Mol. Evol. 45 473–484. - PubMed
  52.  
    1. Mehta S., Mishra B., Sahani M. (2006). Genetic differentiation of Indian camel (Camelus dromedarius) breeds using random oligonucleotide primers. Anim. Genet. Resourc. 39 77–88. 10.1017/S1014233900002157 - DOI
  53.  
    1. Ming L., Yi L., Sa R., Wang Z. X., Wang Z., Ji R. (2017). Genetic diversity and phylogeographic structure of Bactrian camels shown by mitochondrial sequence variations. Anim. Genet. 48 217–220. 10.1111/age.12511 - DOI - PMC - PubMed
  54.  
    1. Mitchell D., Maloney S. K., Jessen C., Laburn H. P., Kamerman P. R., Mitchell G., et al. (2002). Adaptive heterothermy and selective brain cooling in arid-zone mammals. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 131 571–585. 10.1016/S1096-4959(02)00012-X - DOI - PubMed
  55.  
    1. Naderi S., Rezaei H.-R., Pompanon F., Blum M. G., Negrini R., Naghash H.-R., et al. (2008). The goat domestication process inferred from large-scale mitochondrial DNA analysis of wild and domestic individuals. Proc. Natl. Acad. Sci. U.S.A. 105 17659–17664. - PMC - PubMed
  56.  
    1. Nei M. (1987). Molecular Evolutionary Genetics. New York, NY: Columbia university press.
  57.  
    1. Oksanen J., Blanchet F. G., Kindt R., Legendre P., Minchin P. R., O’hara R., et al. (2013). Package ‘vegan’. Commun. Ecol. Pack. Vers. 2 1–295.
  58.  
    1. Orlando L. (2016). Back to the roots and routes of dromedary domestication. Proc. Natl. Acad. Sci. U.S.A. 113 6588–6590. 10.1073/pnas.1606340113 - DOI - PMC - PubMed
  59.  
    1. Oulad Belkhir A., Chehma A., Faye B. (2013). Phenotypic variability of two principal Algerian camel’s populations (Targui and Sahraoui). Emirates J. Food Agric. 25 231–237.
  60.  
    1. Paradis E. (2010). pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26 419–420. - PubMed
  61.  
    1. Porter V., Alderson L., Hall S. J., Sponenberg D. P. (2016). Mason’s World Encyclopedia of Livestock Breeds and Breeding, 2 Volume Pack. Wallingford: CABI.
  62.  
    1. Posada D. (2008). jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25 1253–1256. 10.1093/molbev/msn083 - DOI - PubMed
  63.  
    1. R Development Core Team (2018). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.
  64.  
    1. Rambaut A., Drummond A. J., Xie D., Baele G., Suchard M. A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67 901–904. - PMC - PubMed
  65.  
    1. Ronquist F., Teslenko M., van der Mark P., Ayres D. L., Darling A., Höhna S., et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61 539–542. 10.1093/sysbio/sys029 - DOI - PMC - PubMed
  66.  
    1. Rozas J., Ferrer-Mata A., Sánchez-DelBarrio J. C., Guirao-Rico S., Librado P., Ramos-Onsins S. E., et al. (2017). DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34 3299–3302. 10.1093/molbev/msx248 - DOI - PubMed
  67.  
    1. Saad Y. M., El Hanafy A. A., Alkarim S. A., Almehdar H. A., Redwan E. M. (2017). Analysis of genetic variations in camel breeds (Camelus dromedarius). World Acad. Sci. Eng. Technol. Int. J. Biol. Biomol. Agric. Food Biotechnol. Eng. 11 564–568.
  68.  
    1. Schmidt-Nielsen B., Schmidt-Nielsen K., Houpt T. R., Jarnum S. A. (1956). Water balance of the camel. Am. J. Physiol. Legacy Content 185 185–194. 10.1152/ajplegacy.1956.185.1.185 - DOI - PubMed
  69.  
    1. Stoneking M., Hedgecock D., Higuchi R. G., Vigilant L., Erlich H. A. (1991). Population variation of human mtDNA control region sequences detected by enzymatic amplification and sequence-specific oligonucleotide probes. Am. J. Hum. Genet. 48 370–382. - PMC - PubMed
  70.  
    1. Uerpmann H.-P., Uerpmann M. (2002). The appearance of the domestic camel in south-east Arabia. J. Oman Stud. 12 23 5–260.
  71.  
    1. Yang L., Kong X., Yang S., Dong X., Yang J., Gou X., et al. (2018). Haplotype diversity in mitochondrial DNA reveals the multiple origins of Tibetan horse. PLoS One 13:e0201564. 10.1371/journal.pone.0201564 - DOI - PMC - PubMed

Page Navigation