Genetics; Animal Science and Zoology; General Medicine; Ecology, Evolution, Behavior and Systematics
Abstract :
[en] [en] BACKGROUND: Cattle populations harbor generally high inbreeding levels that can lead to inbreeding depression (ID). Here, we study ID with different estimators of the inbreeding coefficient F, evaluate their sensitivity to used allele frequencies (founder versus sample allele frequencies), and compare effects from recent and ancient inbreeding.
METHODS: We used data from 14,205 Belgian Blue beef cattle genotyped cows that were phenotyped for 11 linear classification traits. We computed estimators of F based on the pedigree information (FPED), on the correlation between uniting gametes (FUNI), on the genomic relationship matrix (FGRM), on excess homozygosity (FHET), or on homozygous-by-descent (HBD) segments (FHBD).
RESULTS: FUNI and FGRM were sensitive to used allele frequencies, whereas FHET and FHBD were more robust. We detected significant ID for four traits related to height and length; FHBD and FUNI presenting the strongest associations. Then, we took advantage of the classification of HBD segments in different age-related classes (the length of an HBD segment being inversely related to the number of generations to the common ancestors) to determine that recent HBD classes (common ancestors present approximately up to 15 generations in the past) presented stronger ID than more ancient HBD classes. We performed additional analyses to check whether these observations could result from a lower level of variation in ancient HBD classes, or from a reduced precision to identify these shorter segments.
CONCLUSIONS: Overall, our results suggest that mutational load decreases with haplotype age, and that mating plans should consider mainly the levels of recent inbreeding.
Disciplines :
Animal production & animal husbandry Veterinary medicine & animal health Genetics & genetic processes
Author, co-author :
Naji, Maulana ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA)
Gualdrón Duarte, José Luis; Unit of Animal Genomics, GIGA-R & Faculty of Veterinary Medicine, University of Liège, Quartier Hôpital, Avenue de l'Hôpital, 11, 4000, Liege, Belgium ; Walloon Breeders Association (awe groupe), 5590, Ciney, Belgium
Forneris, Natalia ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA)
Druet, Tom ; Université de Liège - ULiège > GIGA > GIGA Medical Genomics - Unit of Animal Genomics ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA)
Language :
English
Title :
Inbreeding depression is associated with recent homozygous-by-descent segments in Belgian Blue beef cattle.
Publication date :
2024
Journal title :
Genetics, Selection, Evolution
ISSN :
0999-193X
eISSN :
1297-9686
Publisher :
Springer Science and Business Media LLC, France
Volume :
56
Issue :
1
Pages :
10
Peer reviewed :
Peer Reviewed verified by ORBi
Tags :
CÉCI : Consortium des Équipements de Calcul Intensif
Charlier C, Coppieters W, Rollin F, Desmecht D, Agerholm JS, Cambisano N, et al. Highly effective SNP-based association mapping and management of recessive defects in livestock. Nat Genet. 2008;40:449–54. DOI: 10.1038/ng.96
Hedrick PW, Kalinowski ST. Inbreeding depression in conservation biology. Annu Rev Ecol Evol Syst. 2000;31:139–62. DOI: 10.1146/annurev.ecolsys.31.1.139
Hedrick PW, Garcia-Dorado A. Understanding inbreeding depression, purging, and genetic rescue. Trends Ecol Evol. 2016;31:940–52. DOI: 10.1016/j.tree.2016.09.005
Leroy G. Inbreeding depression in livestock species: review and meta-analysis. Anim Genet. 2014;45:618–28. DOI: 10.1111/age.12178
Malécot G. Mathématiques de l’hérédité. Paris: Masson & Cie; 1948.
Wang J. Pedigrees or markers: which are better in estimating relatedness and inbreeding coefficient? Theor Popul Biol. 2016;107:4–13. DOI: 10.1016/j.tpb.2015.08.006
Keller MC, Visscher PM, Goddard ME. Quantification of inbreeding due to distant ancestors and its detection using dense single nucleotide polymorphism data. Genetics. 2011;189:237–49. DOI: 10.1534/genetics.111.130922
Nietlisbach P, Muff S, Reid JM, Whitlock MC, Keller LF. Nonequivalent lethal equivalents: models and inbreeding metrics for unbiased estimation of inbreeding load. Evol Appl. 2018;12:266–79. DOI: 10.1111/eva.12713
Yengo L, Zhu Z, Wray NR, Weir BS, Yang J, Robinson MR, et al. Detection and quantification of inbreeding depression for complex traits from SNP data. Proc Natl Acad Sci USA. 2017;114:8602–7. DOI: 10.1073/pnas.1621096114
Alemu SW, Kadri NK, Harland C, Faux P, Charlier C, Caballero A, et al. An evaluation of inbreeding measures using a whole-genome sequenced cattle pedigree. Heredity. 2021;126:410–23. DOI: 10.1038/s41437-020-00383-9
Caballero A, Villanueva B, Druet T. On the estimation of inbreeding depression using different measures of inbreeding from molecular markers. Evol Appl. 2021;14:416–28. DOI: 10.1111/eva.13126
Leutenegger A-L, Prum B, Génin E, Verny C, Lemainque A, Clerget-Darpoux F, et al. Estimation of the inbreeding coefficient through use of genomic data. Am J Hum Genet. 2003;73:516–23. DOI: 10.1086/378207
Vieira FG, Albrechtsen A, Nielsen R. Estimating IBD tracts from low coverage NGS data. Bioinformatics. 2016;32:2096–102. DOI: 10.1093/bioinformatics/btw212
Narasimhan V, Danecek P, Scally A, Xue Y, Tyler-Smith C, Durbin R. BCFtools/RoH: a hidden Markov model approach for detecting autozygosity from next-generation sequencing data. Bioinformatics. 2016;32:1749–51. DOI: 10.1093/bioinformatics/btw044
Druet T, Gautier M. A model-based approach to characterize individual inbreeding at both global and local genomic scales. Mol Ecol. 2017;26:5820–41. DOI: 10.1111/mec.14324
Thompson EA. Identity by descent: variation in meiosis, across genomes, and in populations. Genetics. 2013;194:301–26. DOI: 10.1534/genetics.112.148825
Kirin M, McQuillan R, Franklin CS, Campbell H, McKeigue PM, Wilson JF. Genomic runs of homozygosity record population history and consanguinity. PLoS One. 2010;5:e13996. DOI: 10.1371/journal.pone.0013996
Pemberton TJ, Absher D, Feldman MW, Myers RM, Rosenberg NA, Li JZ. Genomic patterns of homozygosity in worldwide human populations. Am J Hum Genet. 2012;91:275–92. DOI: 10.1016/j.ajhg.2012.06.014
Ceballos FC, Joshi PK, Clark DW, Ramsay M, Wilson JF. Runs of homozygosity: windows into population history and trait architecture. Nat Rev Genet. 2018;19:220–34. DOI: 10.1038/nrg.2017.109
Doekes HP, Veerkamp RF, Bijma P, de Jong G, Hiemstra SJ, Windig JJ. Inbreeding depression due to recent and ancient inbreeding in Dutch Holstein-Friesian dairy cattle. Genet Sel Evol. 2019;51:54. DOI: 10.1186/s12711-019-0497-z
Makanjuola BO, Maltecca C, Miglior F, Schenkel FS, Baes CF. Effect of recent and ancient inbreeding on production and fertility traits in Canadian Holsteins. BMC Genomics. 2020;21:605. DOI: 10.1186/s12864-020-07031-w
Stoffel MA, Johnston SE, Pilkington JG, Pemberton JM. Mutation load decreases with haplotype age in wild Soay sheep. Evol Lett. 2021;5:187–95. DOI: 10.1002/evl3.229
Gualdrón Duarte JL, Yuan C, Gori A-S, Moreira GCM, Takeda H, Coppieters W, et al. Sequenced-based GWAS for linear classification traits in Belgian Blue beef cattle reveals new coding variants in genes regulating body size in mammals. Genet Sel Evol. 2023;55:83. DOI: 10.1186/s12711-023-00857-4
Li CC, Horvitz DG. Some methods of estimating the inbreeding coefficient. Am J Hum Genet. 1953;5:107–17.
Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007;81:559–75. DOI: 10.1086/519795
Yang J, Lee SH, Goddard ME, Visscher PM. GCTA: a tool for genome-wide complex trait analysis. Am J Hum Genet. 2011;88:76–82. DOI: 10.1016/j.ajhg.2010.11.011
Bertrand AR, Kadri NK, Flori L, Gautier M, Druet T. RZooRoH: an R package to characterize individual genomic autozygosity and identify homozygous-by-descent segments. Methods Ecol Evol. 2019;10:860–6. DOI: 10.1111/2041-210X.13167
Druet T, Gautier M. A hidden Markov model to estimate homozygous-by-descent probabilities associated with nested layers of ancestors. Theor Popul Biol. 2022;145:38–51. DOI: 10.1016/j.tpb.2022.03.001
Gengler N, Mayeres P, Szydlowski M. A simple method to approximate gene content in large pedigree populations: application to the myostatin gene in dual-purpose Belgian Blue cattle. Animal. 2007;1:21–8. DOI: 10.1017/S1751731107392628
Misztal I, Tsuruta S, Strabel T, Auvray B, Druet T, Lee DH. BLUPF90 and related programs (BGF90). In: Proceedings of the 7th world congress on genetics applied to livestock production: 19–23 August 2002; Montpellier. 2002.
Caballero A, Fernández A, Villanueva B, Toro MA. A comparison of marker-based estimators of inbreeding and inbreeding depression. Genet Sel Evol. 2022;54:82. DOI: 10.1186/s12711-022-00772-0
Solé M, Gori A-S, Faux P, Bertrand A, Farnir F, Gautier M, et al. Age-based partitioning of individual genomic inbreeding levels in Belgian Blue cattle. Genet Sel Evol. 2017;49:92. DOI: 10.1186/s12711-017-0370-x
Druet T, Pérez-Pardal L, Charlier C, Gautier M. Identification of large selective sweeps associated with major genes in cattle. Anim Genet. 2013;44:758–62. DOI: 10.1111/age.12073
Gautier M, Vitalis R. Inferring population histories using genome-wide allele frequency data. Mol Biol Evol. 2013;30:654–68. DOI: 10.1093/molbev/mss257
Szpiech ZA, Xu J, Pemberton TJ, Peng W, Zöllner S, Rosenberg NA, et al. Long runs of homozygosity are enriched for deleterious variation. Am J Hum Genet. 2013;93:90–102. DOI: 10.1016/j.ajhg.2013.05.003
Kiezun A, Pulit SL, Francioli LC, van Dijk F, Swertz M, Boomsma DI, et al. Deleterious alleles in the human genome are on average younger than neutral alleles of the same frequency. PLoS Genet. 2013;9: e1003301. DOI: 10.1371/journal.pgen.1003301
Santiago E, Novo I, Pardiñas AF, Saura M, Wang J, Caballero A. Recent demographic history inferred by high-resolution analysis of linkage disequilibrium. Mol Biol Evol. 2020;37:3642–53. DOI: 10.1093/molbev/msaa169
Hayes BJ, Visscher PM, McPartlan HC, Goddard ME. Novel multilocus measure of linkage disequilibrium to estimate past effective population size. Genome Res. 2003;13:635–43. DOI: 10.1101/gr.387103
Boitard S, Rodríguez W, Jay F, Mona S, Austerlitz F. Inferring population size history from large samples of genome-wide molecular data-an approximate Bayesian computation approach. PLoS Genet. 2016;12: e1005877. DOI: 10.1371/journal.pgen.1005877