Advertisement

Genetic diversity of Nubian ibex in comparison to other ibex and domesticated goat species

  • Lubna M. A. Hassan
  • Danny Arends
  • Siham A. Rahmatalla
  • Monika Reissmann
  • Henry Reyer
  • Klaus Wimmers
  • Sumaia M. A. Abukashawa
  • Gudrun A. Brockmann
Original Article

Abstract

Capra nubiana is a wild ibex species that is in danger of extinction. This study aimed at assessing the genetic diversity and population structure of Nubian ibex (Capra nubiana, n = 8) in comparison to Alpine ibex (Capra ibex, n = 8), Bezoar ibex (Capra aegagrus, n = 4), and domesticated Taggar goats (Capra aegagrus hircus, n = 24). All animals were genotyped with the 50K goat SNP chip. Since commercial SNP chips are not designed for wild species, data analysis was done in two ways: (1) using all callable SNPs (33,698) and (2) with a reduced set of SNPs segregating within three out of four populations (662). Using these two sets of SNPs, the observed heterozygosity in Nubian ibex ranged from 0.02 to 0.44, in Alpine ibex from 0.01 to 0.38, and in Bezoar ibex from 0.13 to 0.38, when analyzing 33,698 or 662 SNPs, respectively. In domesticated Taggar goats, the values for the observed heterozygosity using all 33,698 callable SNPs and the reduced set of 662 SNPs were similar (0.40–0.41). Pairwise FST values for the differentiation between species ranged from 0.17–0.35 (Bezoar ibex vs. Taggar goats) to 0.47–0.91 (Bezoar vs. Alpine ibex), and was 0.33–0.90 between Bezoar and Nubian ibex, respectively, to the two sets of SNPs. The analysis of molecular variance among all animals revealed that 74–78% can be explained by differences between species, while the residual 22–26% result from differences among individuals, respectively. Cluster analysis of Nei’s genetic distance allowed to detected two distinct clusters comprising Nubian and Alpine ibex on one hand and Taggar goats and Bezoar ibex on the other hand, and clear separation of all four breeds. Principal component (PC) analysis confirmed and further refined the clusters. SNPs that contributed most to PC1 allowed us to identify genomic regions accounting for the distances between species. These regions contain known milk protein genes. The identification of milk protein genes as contributors to the differentiation between species provides insights into the domestication of wild Capra breeds.

Keywords

Genetic diversity Nubian ibex Alpine ibex Bezoar ibex Goat Conservation 

Notes

Acknowledgments

We acknowledge the help with collecting animal material of Nubian ibex from Wildlife Research Center researchers and drivers especially from Dinder Wildlife Research Station. We also thank the Wildlife Conservation General Administration in Khartoum and Red Sea State as well as the managers of the local communities in the Red Sea State. The samples of Bezoar and Alpine ibex were provided by the DNA and tissue bank of the Leibniz Institute for Zoo and Wildlife Research Berlin, Germany. LMAH was partially supported by the Wildlife Research Center, Sudan, and through a scholarship of the Humboldt-Universität zu Berlin, Germany. S.A.R. is a fellow of the Alexander von Humboldt Foundation.

Authors’ contributions

L.M.A.H. provided ibex samples, contributed to the study design, DNA extraction, contributed to the manuscript.

D.A. performed the data analysis and drafted the manuscript.

S.A.R. provided Taggar goat samples, contributed to the data analysis and writing the manuscript.

M.R. developed and refined the protocols for DNA extraction, contributed samples from different ibex, and contributed to the manuscript.

H.R. performed the SNP chip hybridization, genotype calling, and initial data check.

K.W. contributed to genotyping.

S.M.A.A. contributed to develop the study.

G.A.B. supervised the study through development of the study design, critical data analysis, discussing the data and results, and finalizing the manuscript.

Compliance with ethical standards

Competing interest

The authors declare no conflict of interest.

Supplementary material

10344_2018_1212_MOESM1_ESM.txt (3.4 mb)
ESM 1 Locations of protein coding gene (TXT 3463 kb)
10344_2018_1212_MOESM2_ESM.xlsx (9 kb)
ESM 2 Estimates of pairwise genetic differentiation (FST) between species using StAMMP R package (XLSX 8 kb)
10344_2018_1212_MOESM3_ESM.xlsx (8 kb)
ESM 3 AMOVA (XLSX 7 kb)
10344_2018_1212_MOESM4_ESM.png (22 kb)
ESM 4 Euclidean distance (PNG 22 kb)
10344_2018_1212_MOESM5_ESM.xlsx (17 kb)
ESM 5 Structure (XLSX 16 kb)
10344_2018_1212_MOESM6_ESM.png (54 kb)
ESM 6 Genomic location of SNPs with high contribution to PC1, PC2, and PC3 (PNG 54 kb)
10344_2018_1212_MOESM7_ESM.xlsx (89 kb)
ESM 7 SNPs and genes contributing to PC1, PC2, and PC3 (XLSX 89 kb)

References

  1. Albrechtsen A, Nielsen FC, Nielsen R (2010) Ascertainment biases in SNP chips affect measures of population divergence. Mol Biol Evol 27:2534–2547.  https://doi.org/10.1093/molbev/msq148 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alkon PU et al (2008) Capra nubiana (Nubian Ibex). International Union for Conservation of Nature. http://www.iucnredlist.org/details/3796/0. Accessed 2018–02-06
  3. Biebach I, Keller LF (2009) A strong genetic footprint of the re-introduction history of alpine ibex (Capra ibex ibex). Mol Ecol 18:5046–5058.  https://doi.org/10.1111/j.1365-294X.2009.04420.x CrossRefPubMedGoogle Scholar
  4. Bushara I, Abu Nikhaila MMAA (2012) Productivity performance of Taggar female kids under grazing condition. J Anim Prod Adv 2:74–79Google Scholar
  5. Butynski T, Happold D, Happold M, Hoffmann M (2013) Mammals of Africa, vol IV. Bloomsbury Publishing, LondonGoogle Scholar
  6. Castelló JR (2016) Bovids of the world: antelopes, gazelles, cattle, goats, sheep, and relatives. Princeton University Press, PrincetonCrossRefGoogle Scholar
  7. El-Naim Y (1979) Some reproductive and productive traits of Sudan nubian goats. MVSc dissertation, University of Khartoum, SudanGoogle Scholar
  8. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578.  https://doi.org/10.1111/j.1471-8286.2007.01758.x CrossRefPubMedPubMedCentralGoogle Scholar
  9. Grubb P (2005) Order artiodactyla. In: Wilson DE, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference, vol 1/2, 3rd edn. The Johns Hopkins University Press, Baltimore, pp 637–722Google Scholar
  10. Grzimek B, Zingg R (1990) Alpine ibex (Capra ibex ibex). In: Parker SP (ed) Grzimek's encyclopedia of mammals, vol 5, 3rd edn. McGraw-Hill, New York, pp 516–523Google Scholar
  11. HCENR (2014) Fifth National Report to the convention on biological diversity (CBD). Ministry of Environment, Forestry and Physical Development, SudanGoogle Scholar
  12. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332.  https://doi.org/10.1111/j.1755-0998.2009.02591.x CrossRefPubMedPubMedCentralGoogle Scholar
  13. IUCN (2018) The IUCN Red List of Threatened Species, 2017—3rd edn. International Union for Conservation of Nature, http://www.iucnredlist.org
  14. Johnson AD, Handsaker RE, Pulit SL, Nizzari MM, O'Donnell CJ, de Bakker PI (2008) SNAP: a web-based tool for identification and annotation of proxy SNPs using HapMap. Bioinformatics 24:2938–2939.  https://doi.org/10.1093/bioinformatics/btn564 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) diveRsity: an R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4:782–788CrossRefGoogle Scholar
  16. Kijas JW, Ortiz JS, McCulloch R, James A, Brice B, Swain B, Tosser-Klopp G, the International Goat Genome Consortium (2013) Genetic diversity and investigation of polledness in divergent goat populations using 52 088 SNPs. Anim Genet 44:325–335.  https://doi.org/10.1111/age.12011 CrossRefPubMedGoogle Scholar
  17. Lashmar SF, Visser C, van Marle-Köster E (2015) Validation of the 50k Illumina goat SNP chip in the South African Angora goat. South African J Anim Sci 45:56–59.  https://doi.org/10.4314/sajas.v45i1.7 CrossRefGoogle Scholar
  18. Liu N, Chen L, Wang S, Oh C, Zhao H (2005) Comparison of single-nucleotide polymorphisms and microsatellites in inference of population structure. BMC Genet 6(Suppl 1):S26.  https://doi.org/10.1186/1471-2156-6-S1-S26 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Malomane DK, Reimer C, Weigend S, Weigend A, Sharifi AR, Simianer H (2018) Efficiency of different strategies to mitigate ascertainment bias when using SNP panels in diversity studies. BMC Genomics 19:22.  https://doi.org/10.1186/s12864-017-4416-9 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Mendelssohn H (1990) Nubian ibex (Capra ibex nubiana). In: Parker SP (ed) In Grzimek's encyclopedia of mammals, vol 5. McGraw-Hill, New York, pp 525–527Google Scholar
  21. Miller JM, Kijas JW, Heaton MP, McEwan JC, Coltman DW (2012) Consistent divergence times and allele sharing measured from cross-species application of SNP chips developed for three domestic species. Mol Ecol Resour 12:1145–1150.  https://doi.org/10.1111/1755-0998.12017 CrossRefPubMedGoogle Scholar
  22. Muffarah MB (1995) Goat breeds and varieties in Sudan. Proceeding of Training Course, Sheep and Goat Production, Arab Centre for Studies of Arid and Dryland (ACSAD), Khartoum 17–27 January, SudanGoogle Scholar
  23. Nei M (1972) Genetic distance between populations. Am Nat 106:283–292CrossRefGoogle Scholar
  24. Nielsen R (2004) Population genetic analysis of ascertained SNP data. Hum Genomics 1:218–224CrossRefPubMedPubMedCentralGoogle Scholar
  25. Nimir MB (1997) Sudan—chapter 4–11. IUCN/SSC Caprinae Specialist Group, IUCN, Gland, Switzerland and Cambridge, UKGoogle Scholar
  26. Nowak RM (1999) Walker’s mammals of the world, vol 1. The John Hopkins University Press, BaltimoreGoogle Scholar
  27. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290CrossRefPubMedGoogle Scholar
  28. Pembleton L, Cogan N, Forste J (2013) Statistical analysis of mixed ploidy populations. Mol Ecol Resour 13:946–952.  https://doi.org/10.1111/1755-0998.12129 CrossRefPubMedGoogle Scholar
  29. Porter V, Alderson L, Hall SJG, Sponenberg DP (2016) Mason's world encyclopedia of livestock breeds and breeding, vol 1, 6th edn. CABI, WallingfordCrossRefGoogle Scholar
  30. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  31. Rahmatalla SA, Arends D, Reissmann M, Said Ahmed A, Wimmers K, Reyer H, Brockmann GA (2017) Whole genome population genetics analysis of Sudanese goats identifies regions harboring genes associated with major traits. BMC Genet 18:92.  https://doi.org/10.1186/s12863-017-0553-z CrossRefPubMedPubMedCentralGoogle Scholar
  32. Scherf BD (2000) World watch list for domestic animal diversity vol, 3rd edn. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  33. Shackleton DM (1997) Wild sheep and goats and their relatives: status survey and conservation action plan for Caprinae IUCN/SSC Caprinae specialist group. IUCN, GlandGoogle Scholar
  34. Stuart C, Stuart T (2016) Mammals of North Africa and the Middle East. Bloomsbury Publishing, LondonGoogle Scholar
  35. Stüwe M, Nievergelt B (1991) Recovery of alpine ibex from near extinction: the result of effective protection, captive breeding, and reintroductions. Appl Anim Behav Sci 29:379–387.  https://doi.org/10.1016/0168-1591(91)90262-V CrossRefGoogle Scholar
  36. Talenti A, Nicolazzi EL, Chessa S, Frattini S, Moretti R, Coizet B, Nicoloso L, Colli L, Pagnacco G, Stella A, Ajmone-Marsan P, Ptak G, Crepaldi P (2016) A method for single nucleotide polymorphism selection for parentage assessment in goats. J Dairy Sci 99:3646–3653.  https://doi.org/10.3168/jds.2015-10077 CrossRefPubMedGoogle Scholar
  37. TheRCoreTeam (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  38. Tosser-Klopp G, Bardou P, Bouchez O, Cabau C, Crooijmans R, Dong Y (2014) Design and characterization of a 52K SNP chip for goats. PLoS One 9:e86227.  https://doi.org/10.1371/journal.pone.0086227 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Tosser-Klopp G, Bardou P, Bouchez O, Cabau C, Crooijmans R, Dong Y, Donnadieu-Tonon C, Eggen A, Heuven HCM, Jamli S, Jiken AJ, Klopp C, Lawley CT, McEwan J, Martin P, Moreno CR, Mulsant P, Nabihoudine I, Pailhoux E, Palhière I, Rupp R, Sarry J, Sayre BL, Tircazes A, Wang J, Wang W, Zhang W, International Goat Genome Consortium (2016) Correction: design and characterization of a 52K SNP Chip for goats. PLoS One 11:e0152632.  https://doi.org/10.1371/journal.pone.0152632 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Wilson T (1991) Small ruminant production and the small ruminant genetic resource in tropical Africa FAO animal production and health paper 88Google Scholar
  41. Wright S (1969) Evolution and the genetics of populations, vol 2: the theory of gene frequencies. The University of Chicago Press, Chicago and LondonGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Lubna M. A. Hassan
    • 1
    • 2
  • Danny Arends
    • 3
  • Siham A. Rahmatalla
    • 3
    • 4
  • Monika Reissmann
    • 3
  • Henry Reyer
    • 5
  • Klaus Wimmers
    • 5
  • Sumaia M. A. Abukashawa
    • 2
  • Gudrun A. Brockmann
    • 3
  1. 1.Wildlife Research Center, Animal Resource Research CorporationFederal Ministry of Livestock, Fisheries and RangelandsKhartoumSudan
  2. 2.Faculty of Sciences, Department of ZoologyUniversity of KhartoumKhartoumSudan
  3. 3.Albrecht Daniel Thaer-Institute for Agricultural and Horticultural SciencesHumboldt-Universität zu BerlinBerlinGermany
  4. 4.Faculty of Animal Production, Department of Dairy ProductionUniversity of KhartoumKhartoum NorthSudan
  5. 5.Institute for Genome BiologyLeibniz Institute for Farm Animal Biology (FBN)DummerstorfGermany

Personalised recommendations