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Genetic insights into crossbred dairy cattle of Pakistan: exploring allele frequency, linkage disequilibrium, and effective population size at a genome-wide scale

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Abstract

Linkage disequilibrium (LD) affects genomic studies accuracy. High-density genotyping platforms identify SNPs across animal genomes, increasing LD evaluation resolution for accurate analysis. This study aimed to evaluate the decay and magnitude of LD in a cohort of 81 crossbred dairy cattle using the GGP_HDv3_C Bead Chip. After quality control, 116,710 Single Nucleotide Polymorphisms (SNPs) across 2520.241 Mb of autosomes were retained. LD extent was assessed between autosomal SNPs within a 10 Mb range using the r2 statistics. LD value declined as inter-marker distance increased. The average r2 value was 0.24 for SNP pairs < 10 kb apart, decreasing to 0.13 for 50–100 kb distances. Minor allele frequency (MAF) and sample size significantly impact LD. Lower MAF thresholds result in smaller r2 values, while higher thresholds show increased r2 values. Additionally, smaller sample sizes exhibit higher average r2 values, especially for larger physical distance intervals (> 50 kb) between SNP pairs. Effective population size and inbreeding coefficient were 150 and 0.028 for the present generation, indicating a decrease in genetic diversity over time. These findings imply that the utilization of high-density SNP panels and customized/breed-specific SNP panels represent a highly favorable approach for conducting genome-wide association studies (GWAS) and implementing genomic selection (GS) in the Bos indicus cattle breeds, whose genomes are still largely unexplored. Furthermore, it is imperative to devise a meticulous breeding strategy tailored to each herd, aiming to enhance desired traits while simultaneously preserving genetic diversity.

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References

  • Ardlie KG, Kruglyak L, Seielstad M (2002) Patterns of linkage disequilibrium in the human genome. Nat Rev Genet 3:299–309

    CAS  PubMed  Google Scholar 

  • Bang NN, Hayes BJ, Lyons RE, Randhawa IA, Gaughan JB, McNeill DM (2022) Genomic diversity and breed composition of Vietnamese smallholder dairy cows. J Anim Breed Genet 139:145–160

    CAS  PubMed  Google Scholar 

  • Barbato M, Orozco-Terwengel P, Tapio M, Bruford MW (2015) SNeP: a tool to estimate trends in recent effective population size trajectories using genome-wide SNP data. Front Genet 6:109

    PubMed  PubMed Central  Google Scholar 

  • Barbato M, Hailer F, Upadhyay M, del Corvo M, Colli L, Negrini R, Kim E-S, Crooijmans RP, Sonstegard T, Ajmone-Marsan P (2020) Adaptive introgression from indicine cattle into white cattle breeds from Central Italy. Sci Rep 10:1–11

    Google Scholar 

  • Bebe BO, Udo HM, Rowlands GJ, Thorpe W (2003) Smallholder dairy systems in the Kenya highlands: breed preferences and breeding practices. Livest Prod Sci 82:117–127

    Google Scholar 

  • Bohmanova J, Sargolzaei M, Schenkel FS (2010) Characteristics of linkage disequilibrium in North American Holsteins. BMC Genomics 11:1–11

    Google Scholar 

  • Bolormaa S, Hayes B, Savin K, Hawken R, Barendse W, Arthur P, Herd R, Goddard M (2011) Genome-wide association studies for feedlot and growth traits in cattle. J Anim Sci 89:1684–1697

    CAS  PubMed  Google Scholar 

  • Chen Y, Lin C-H, Sabatti C (2006) Volume measures for linkage disequilibrium. BMC Genet 7:1–8

    Google Scholar 

  • Chhotaray S, Panigrahi M, Pal D, Ahmad SF, Bhanuprakash V, Kumar H, Parida S, Bhushan B, Gaur G, Mishra B (2021) Genome-wide estimation of inbreeding coefficient, effective population size and haplotype blocks in Vrindavani crossbred cattle strain of India. Biol Rhythm Res 52:666–679

    CAS  Google Scholar 

  • Corbin LJ, Liu A, Bishop S, Woolliams J (2012) Estimation of historical effective population size using linkage disequilibria with marker data. J Anim Breed Genet 129:257–270

    CAS  PubMed  Google Scholar 

  • Crow J, Kimura M (1970) An introduction to population genetics theory. Harper & Row, New York

    Google Scholar 

  • Deng T, Liang A, Liu J, Hua G, Ye T, Liu S, Campanile G, Plastow G, Zhang C, Wang Z (2019) Genome-wide SNP data revealed the extent of linkage disequilibrium, persistence of phase and effective population size in purebred and crossbred buffalo populations. Front Genet 9:688

    PubMed  PubMed Central  Google Scholar 

  • Dezetter C, Leclerc H, Mattalia S, Barbat A, Boichard D, Ducrocq V (2015) Inbreeding and crossbreeding parameters for production and fertility traits in Holstein, Montbéliarde, and Normande cows. J Dairy Sci 98:4904–4913

    CAS  PubMed  Google Scholar 

  • Doekes HP, Veerkamp RF, Bijma P, Hiemstra SJ, Windig JJ (2018) Trends in genome-wide and region-specific genetic diversity in the Dutch-Flemish Holstein-Friesian breeding program from 1986 to 2015. Genet Sel Evol 50:1–16

    Google Scholar 

  • Elavarasan K, Kumar S, Agarwal S, Vani A, Sharma R, Kumar S, Chauhan A, Sahoo NR, Verma MR, Gaur GK (2023) Estimation of microsatellite-based autozygosity and its correlation with pedigree inbreeding coefficient in crossbred cattle. Animal Biotechnol 2023:1–14

    Google Scholar 

  • Espigolan R, Baldi F, Boligon AA, Souza FR, Gordo DG, Tonussi RL, Cardoso DF, Oliveira HN, Tonhati H, Sargolzaei M (2013) Study of whole genome linkage disequilibrium in Nellore cattle. BMC Genomics 14:1–8

    Google Scholar 

  • Gibbs RA, Taylor JF, van Tassell CP, Barendse W, Eversole KA, Gill CA, Green RD, Hamernik DL, Kappes SM (2009) Genome-wide survey of SNP variation uncovers the genetic structure of cattle breeds. Science 324:528–532

    CAS  PubMed  Google Scholar 

  • Goddard M (2009) Genomic selection: prediction of accuracy and maximisation of long term response. Genetica 136:245–257

    PubMed  Google Scholar 

  • Goddard M, Hayes B (2012) Genome-wide association studies and linkage disequilibrium in cattle. Bovine Genomics 2012:192–210

    Google Scholar 

  • Howey R, Cordell H (2011) MapThin. http://www.staff.ncl.ac.uk/richard.howey/mapthin/

  • Karimi K, Esmailizadeh Koshkoiyeh A, Gondro C (2015) Comparison of linkage disequilibrium levels in Iranian indigenous cattle using whole genome SNPs data. J Animal Sci Technol 57:1–10

    Google Scholar 

  • Kelleher M, Berry D, Kearney J, McParland S, Buckley F, Purfield D (2017) Inference of population structure of purebred dairy and beef cattle using high-density genotype data. Animal 11:15–23

    CAS  PubMed  Google Scholar 

  • Khatkar MS, Nicholas FW, Collins AR, Zenger KR, Cavanagh JA, Barris W, Schnabel RD, Taylor JF, Raadsma HW (2008) Extent of genome-wide linkage disequilibrium in Australian Holstein-Friesian cattle based on a high-density SNP panel. BMC Genomics 9:1–18

    Google Scholar 

  • Kruglyak L (1999) Prospects for whole-genome linkage disequilibrium mapping of common disease genes. Nat Genetics 22:139–144

    CAS  PubMed  Google Scholar 

  • Kumar S, Alex R, Gaur G, Mukherjee S, Mandal D, Singh U, Tyagi S, Kumar A, Das A, Deb R (2018) Evolution of Frieswal cattle: a crossbred dairy animal of India. Indian J Anim Sci 88:265–275

    Google Scholar 

  • Larmer S, Sargolzaei M, Schenkel F (2014) Extent of linkage disequilibrium, consistency of gametic phase, and imputation accuracy within and across Canadian dairy breeds. J Dairy Sci 97:3128–3141

    CAS  PubMed  Google Scholar 

  • Leroy G, Baumung R, Boettcher P, Scherf B, Hoffmann I (2016) Sustainability of crossbreeding in developing countries; definitely not like crossing a meadow…. Animal 10:262–273

    CAS  PubMed  Google Scholar 

  • Li Y, Kim J-J (2015) Effective population size and signatures of selection using bovine 50K SNP chips in Korean Native Cattle (Hanwoo). Evol Bioinform 11:EBO.S24359

    Google Scholar 

  • Lu D, Sargolzaei M, Kelly M, Li C, Vander Voort G, Wang Z, Plastow G, Moore S, Miller SP (2012) Linkage disequilibrium in Angus, Charolais, and Crossbred beef cattle. Front Genetics 3:152

    Google Scholar 

  • Makanjuola BO, Miglior F, Abdalla EA, Maltecca C, Schenkel FS, Baes CF (2020) Effect of genomic selection on rate of inbreeding and coancestry and effective population size of Holstein and Jersey cattle populations. J Dairy Sci 103:5183–5199

    CAS  PubMed  Google Scholar 

  • Makina S, Taylor J, van Marle-Kö ster E, Muchadeyi FC, Makgahlela ML, MacNeil MD et al (2015) Extent of linkage disequilibrium and effective population size in four South African Sanga cattle breeds. Front Genetics 6:337

    Google Scholar 

  • Martinez R, Bejarano D, Ramírez J, Ocampo R, Polanco N, Perez JE, Onofre HG, Rocha JF (2023) Genomic variability and population structure of six Colombian cattle breeds. Trop Anim Health Prod 55:1–8

    Google Scholar 

  • Matukumalli LK, Lawley CT, Schnabel RD, Taylor JF, Allan MF, Heaton MP, O’Connell J, Moore SS, Smith TP, Sonstegard TS (2009) Development and characterization of a high density SNP genotyping assay for cattle. PLoS ONE 4:e5350

    PubMed  PubMed Central  Google Scholar 

  • Mbole-Kariuki MN, Sonstegard T, Orth A, Thumbi S, Bronsvoort BDC, Kiara H, Toye P, Conradie I, Jennings A, Coetzer K (2014) Genome-wide analysis reveals the ancient and recent admixture history of East African Shorthorn Zebu from Western Kenya. Heredity 113:297–305

    CAS  PubMed  PubMed Central  Google Scholar 

  • McKay SD, Schnabel RD, Murdoch BM, Matukumalli LK, Aerts J, Coppieters W, Crews D, Neto ED, Gill CA, Gao C (2007) Whole genome linkage disequilibrium maps in cattle. BMC Genet 8:1–12

    Google Scholar 

  • Meuwissen TH, Hayes BJ, Goddard M (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157:1819–1829

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mrode R, Ojango JMK, Okeyo A, Mwacharo JM (2019) Genomic selection and use of molecular tools in breeding programs for indigenous and crossbred cattle in developing countries: current status and future prospects. Front Genet 9:694

    PubMed  PubMed Central  Google Scholar 

  • Mumtaz S, Mukherjee A, Pathak P, Parveen K (2021) Effects of inbreeding on performance traits in Karan Fries crossbred cattle. Indian J Anim Sci 91(5):1

    Google Scholar 

  • Murray C, Huerta-Sanchez E, Casey F, Bradley DG (2010) Cattle demographic history modelled from autosomal sequence variation. Philos Trans R Soc B Biol Sci 365:2531–2539

    CAS  Google Scholar 

  • O’Brien AMP, Mészáros G, Utsunomiya YT, Sonstegard TS, Garcia JF, van Tassell CP, Carvalheiro R, da Silva MV, Sölkner J (2014) Linkage disequilibrium levels in Bos indicus and Bos taurus cattle using medium and high density SNP chip data and different minor allele frequency distributions. Livest Sci 166:121–132

    Google Scholar 

  • Ouédraogo D, Ouédraogo-Koné S, Yougbaré B, Soudré A, Zoma-Traoré B, Mészáros G, Khayatzadeh N, Traoré A, Sanou M, Mwai OA (2021) Population structure, inbreeding and admixture in local cattle populations managed by community-based breeding programs in Burkina Faso. J Anim Breed Genet 138:379–388

    PubMed  PubMed Central  Google Scholar 

  • Porto-Neto LR, Kijas JW, Reverter A (2014) The extent of linkage disequilibrium in beef cattle breeds using high-density SNP genotypes. Genet Sel Evol 46:1–5

    Google Scholar 

  • Reich DE, Cargill M, Bolk S, Ireland J, Sabeti PC, Richter DJ, Lavery T, Kouyoumjian R, Farhadian SF, Ward R (2001) Linkage disequilibrium in the human genome. Nature 411:199–204

    CAS  PubMed  Google Scholar 

  • Rodríguez-Ramilo ST, Fernández J, Toro MA, Hernández D, Villanueva B (2015) Genome-wide estimates of coancestry, inbreeding and effective population size in the Spanish Holstein population. PLoS ONE 10:e0124157

    PubMed  PubMed Central  Google Scholar 

  • Saravanan K, Panigrahi M, Kumar H, Parida S, Bhushan B, Gaur G, Kumar P, Dutt T, Mishra B, Singh R (2022) Genome-wide assessment of genetic diversity, linkage disequilibrium and haplotype block structure in Tharparkar cattle breed of India. Anim Biotechnol 33:297–311

    CAS  PubMed  Google Scholar 

  • Sargolzaei M, Schenkel F, Jansen G, Schaeffer L (2008) Extent of linkage disequilibrium in Holstein cattle in North America. J Dairy Sci 91:2106–2117

    CAS  PubMed  Google Scholar 

  • Silva C, Neves H, Queiroz S, Sena J, Pimentel E (2010) Extent of linkage disequilibrium in Brazilian Gyr dairy cattle based on genotypes of AI sires for dense SNP markers. In: Proceedings of the 9th world congress on genetics applied to livestock production: 1–6 August 2010. Leipzig, pp 1–29

  • Singh A, Kumar A, Mehrotra A, Pandey AK, Mishra B, Dutt T (2021) Estimation of linkage disequilibrium levels and allele frequency distribution in crossbred Vrindavani cattle using 50K SNP data. PLoS ONE 16:e0259572

    CAS  PubMed  PubMed Central  Google Scholar 

  • Slifer SH (2018) PLINK: key functions for data analysis. Curr Protocols Human Genet 97:e59

    Google Scholar 

  • Stachowicz K, Sargolzaei M, Miglior F, Schenkel F (2011) Rates of inbreeding and genetic diversity in Canadian Holstein and Jersey cattle. J Dairy Sci 94:5160–5175

    CAS  PubMed  Google Scholar 

  • Team RC (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Tian R, Asadollahpour Nanaie H, Wang X, Dalai B, Zhao M, Wang F, Li H, Yang D, Zhang H, Li Y (2023) Genomic adaptation to extreme climate conditions in beef cattle as a consequence of cross-breeding program. BMC Genomics 24:1–10

    CAS  Google Scholar 

  • Uimari P, Kontkanen O, Visscher PM, Pirskanen M, Fuentes R, Salonen JT (2005) Genome-wide linkage disequilibrium from 100,000 SNPs in the East Finland founder population. Twin Res Hum Genet 8:185–197

    PubMed  Google Scholar 

  • Villa-Angulo R, Matukumalli LK, Gill CA, Choi J, van Tassell CP, Grefenstette JJ (2009) High-resolution haplotype block structure in the cattle genome. BMC Genet 10:1–13

    Google Scholar 

  • Wray NR (2005) Allele frequencies and the r2 measure of linkage disequilibrium: impact on design and interpretation of association studies. Twin Res Human Genet 8:87–94

    Google Scholar 

  • Yan J, Shah T, Warburton ML, Buckler ES, McMullen MD, Crouch J (2009) Genetic characterization and linkage disequilibrium estimation of a global maize collection using SNP markers. PLoS ONE 4:e8451

    PubMed  PubMed Central  Google Scholar 

  • Zhang H, Yin L, Wang M, Yuan X, Liu X (2019) Factors affecting the accuracy of genomic selection for agricultural economic traits in maize, cattle, and pig populations. Front Genet 10:189

    PubMed  PubMed Central  Google Scholar 

  • Zhao H, Nettleton D, Dekkers JC (2007) Evaluation of linkage disequilibrium measures between multi-allelic markers as predictors of linkage disequilibrium between single nucleotide polymorphisms. Genetics Res 89:1–6

    CAS  Google Scholar 

  • Zhao F, Wang G, Zeng T, Wei C, Zhang L, Wang H, Zhang S, Liu R, Liu Z, Du L (2014) Estimations of genomic linkage disequilibrium and effective population sizes in three sheep populations. Livest Sci 170:22–29

    Google Scholar 

  • Zhu M, Zhu B, Wang Y, Wu Y, Xu L, Guo L, Yuan Z, Zhang L, Gao X, Gao H (2013) Linkage disequilibrium estimation of Chinese beef Simmental cattle using high-density SNP panels. Asian Aust J Anim Sci 26:772–779

    CAS  Google Scholar 

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Acknowledgements

We acknowledge the Higher Education Commission, Pakistan for providing funding to the first author for her Ph.D. Studies.

Funding

This study is funded by the Pakistan Agricultural Research Council, Agricultural Linkages Programme (ALP) with Project Identification No. AS 016 titled “Development and application of genomic selection in foreign and local cattle breeds for improvement in dairy-related traits”.

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Authors and Affiliations

  1. Agricultural Biotechnology Division, National Institute for Biotechnology and Genetic Engineering College (NIBGE-C), Faisalabad, Pakistan

    Fakhar un Nisa, Muhammad Asif, Imran Amin, Shahid Mansoor & Zahid Mukhtar

  2. Pakistan Institute of Engineering and Applied Sciences (PIEAS), Nilore, Islamabad, Pakistan

    Fakhar un Nisa, Muhammad Asif, Imran Amin, Shahid Mansoor & Zahid Mukhtar

  3. Department of Animal Breeding and Genetics, University of Veterinary and Animal Sciences, Lahore, Pakistan

    Fakhar un Nisa & Haiba Kaul

  4. Animal Biosciences, International Livestock Research Institute, Nairobi, Kenya

    Raphael Mrode

  5. Animal and Veterinary Sciences, Scotland’s Rural College, Edinburgh, UK

    Raphael Mrode

  6. International Centre for Chemical and Biological Sciences, University of Karachi, Karachi, Pakistan

    Shahid Mansoor

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  1. Fakhar un Nisa
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  2. Haiba Kaul
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  3. Muhammad Asif
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  4. Imran Amin
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Contributions

Conceptualization: FUN, RM. Data curation: FUN, MA. Formal analysis: FUN, HK. Investigation: FUN. Methodology: FUN. Project administration: SM, ZM, IA. Resources: SM, IA. Software: FUN. Supervision: RM, ZM, SM. Visualization: FUN, HK. Writing-original draft: FUN. Writing-review and editing: RM, HK, ZM, MA, SM, IA.

Corresponding author

Correspondence to Zahid Mukhtar.

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The authors declare that they have no conflict of interest.

Ethical approval

To ensure the ethical and humane treatment of animals, the study described in this research paper was approved by the Research Ethics Committee of the National Institute for Biotechnology and Genetic Engineering (NIBGE), Faisalabad, Pakistan on 10-06-2020. During blood collection, a professional veterinarian was there to ensure minimal distress and harm to the animals. Before collecting any samples, the researchers met with the owners of the farm where the animals were housed to explain the purpose of the study and obtain informed consent verbally.

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Nisa, F.u., Kaul, H., Asif, M. et al. Genetic insights into crossbred dairy cattle of Pakistan: exploring allele frequency, linkage disequilibrium, and effective population size at a genome-wide scale. Mamm Genome 34, 602–614 (2023). https://doi.org/10.1007/s00335-023-10019-y

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