Genetic analysis of the modern Australian labradoodle dog breed reveals an excess of the poodle genome

Autoři: Muhammad Basil Ali aff001;  Jacquelyn M. Evans aff001;  Heidi G. Parker aff001;  Jaemin Kim aff001;  Susan Pearce-Kelling aff004;  D. Thad Whitaker aff001;  Jocelyn Plassais aff001;  Qaiser M. Khan aff002;  Elaine A. Ostrander aff001
Působiště autorů: Cancer Genetics and Comparative Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda MD, United States of America aff001;  National Institute for Biotechnology and Genetic Engineering (NIBGE), Jhang Road Faisalabad, Punjab, Pakistan aff002;  Pakistan Institute of Engineering and Applied Sciences (PIEAS), Islamabad, Punjab, Pakistan aff003;  OptiGen, LLC Cornell Business and Technology Park, Ithaca, NY, United States of America aff004
Vyšlo v časopise: Genetic analysis of the modern Australian labradoodle dog breed reveals an excess of the poodle genome. PLoS Genet 16(9): e32767. doi:10.1371/journal.pgen.1008956
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008956


The genomic diversity of the domestic dog is an invaluable resource for advancing understanding of mammalian biology, evolutionary biology, morphologic variation, and behavior. There are approximately 350 recognized breeds in the world today, many established through hybridization and selection followed by intense breeding programs aimed at retaining or enhancing specific traits. As a result, many breeds suffer from an excess of particular diseases, one of many factors leading to the recent trend of “designer breed” development, i.e. crossing purebred dogs from existing breeds in the hope that offspring will be enriched for desired traits and characteristics of the parental breeds. We used a dense panel of 150,106 SNPs to analyze the population structure of the Australian labradoodle (ALBD), to understand how such breeds are developed. Haplotype and admixture analyses show that breeds other than the poodle (POOD) and Labrador retriever (LAB) contributed to ALBD formation, but that the breed is, at the genetic level, predominantly POOD, with all small and large varieties contributing to its construction. Allele frequency analysis reveals that the breed is enhanced for variants associated with a poodle-like coat, which is perceived by breeders to have an association with hypoallergenicity. We observed little enhancement for LAB-specific alleles. This study provides a blueprint for understanding how dog breeds are formed, highlighting the limited scope of desired traits in defining new breeds.

Klíčová slova:

Alleles – Dogs – Haplotypes – Homozygosity – Mammalian genomics – Pets and companion animals – Phylogenetic analysis – Single nucleotide polymorphisms


1. American Kennel Club. The New Complete Dog Book. Prisco CRaAD, editor. Mount Joy, PA: Fox Chapel Publishing; 2017.

2. Rogers CA, Brace AH. The International Encyclopedia of Dogs. First American ed. New York: Howell Book House; 1995.

3. Wilcox B, Walkowicz C. Atlas of Dog Breeds of the World. Neptune City, NJ: T.F.H. Pucli; 1995.

4. Parker HG, Dreger DL, Rimbault M, Davis BW, Mullen AB, Carpintero-Ramirez G, et al. Genomic analyses reveal the influence of geographic origin, migration, and hybridization on modern dog breed development. Cell Rep. 2017;19: 697–708. doi: 10.1016/j.celrep.2017.03.079 28445722

5. Karlsson EK, Lindblad-Toh K. Leader of the pack: Gene mapping in dogs and other model organisms. Nat Rev Genet. 2008;9: 713–24. doi: 10.1038/nrg2382 18714291

6. Boyko AR. The domestic dog: man's best friend in the genomic era. Genome Biol. 2011;12: 216. doi: 10.1186/gb-2011-12-2-216 21338479

7. Akey JM, Ruhe AL, Akey DT, Wong AK, Connelly CF, Madeoy J, et al. Tracking footprints of artificial selection in the dog genome. Proc Natl Acad Sci U S A. 2010;107: 1160–5. doi: 10.1073/pnas.0909918107 20080661

8. Boyko A, Quignon P, Li L, Schoenebeck J, Degenhardt J, Lohmueller K, et al. A simple genetic architecture underlies morphological variation in dogs. PLoS Biol. 2010;8(8):e1000451. doi: 10.1371/journal.pbio.1000451 20711490

9. Vaysse A, Ratnakumar A, Derrien T, Axelsson E, Rosengren Pielberg G, Sigurdsson S, et al. Identification of genomic regions associated with phenotypic variation between dog breeds using selection mapping. PLoS Genetics. 2011;7(10):e1002316. doi: 10.1371/journal.pgen.1002316 22022279

10. Hayward JJ, Castelhano MG, Oliveira KC, Corey E, Balkman C, Baxter TL, et al. Complex disease and phenotype mapping in the domestic dog. Nat Commun. 2016;7: 10460. doi: 10.1038/ncomms10460 26795439

11. Plassais J, Kim J, Davis BW, Karyadi DM, Hogan AN, Harris AC, et al. Whole genome sequencing of canids reveals genomic regions under selection and variants influencing morphology. Nat Commun. 2019;10: 1489. doi: 10.1038/s41467-019-09373-w 30940804

12. Lewis TW, Abhayaratne BM, Blott SC. Trends in genetic diversity for all Kennel Club registered pedigree dog breeds. Canine Genet Epidemiol. 2015;2: 13. doi: 10.1186/s40575-015-0027-4 26401341

13. Bellumori TP, Famula TR, Bannasch DL, Belanger JM, Oberbauer AM. Prevalence of inherited disorders among mixed-breed and purebred dogs: 27,254 cases (1995–2010). J Am Vet Med Assoc. 2013;242: 1549–55. doi: 10.2460/javma.242.11.1549 23683021

14. Sams AJ, Boyko AR. Fine-scale resolution of runs of homozygosity reveal patterns of inbreeding and substantial overlap with recessive disease genotypes in domestic dogs. G3 (Bethesda). 2019;9: 117–23. doi: 10.1534/g3.118.200836 30429214

15. Crispin S. The Advisory Council on the Welfare of Issues of Dog Breeding. Vet J. 2011;189: 129–31. doi: 10.1016/j.tvjl.2011.06.008 21742522

16. Asher L, Diesel G, Summers JF, McGreevy PD, Collins LM. Inherited defects in pedigree dogs. Part 1: Disorders related to breed standards. Vet J. 2009;182: 402–11. doi: 10.1016/j.tvjl.2009.08.033 19836981

17. Fogle B. The New Encyclopedia of the Dog. second ed. New York: Dorling Kindersley Publishing, Inc.; 2000.

18. Pickrell JK, Patterson N, Barbieri C, Berthold F, Gerlach L, Guldemann T, et al. The genetic prehistory of southern Africa. Nat Commun. 2012;3: 1143. doi: 10.1038/ncomms2140 23072811

19. Dreger DL, Rimbault M, Davis BW, Bhatnagar A, Parker HG, Ostrander EA. Whole-genome sequence, SNP chips and pedigree structure: building demographic profiles in domestic dog breeds to optimize genetic-trait mapping. Dis Model Mech. 2016;9: 1445–60. doi: 10.1242/dmm.027037 27874836

20. Dreger DL, Davis BW, Cocco R, Sechi S, Di Cerbo A, Parker HG, et al. Commonalities in development of pure breeds and population isolates revealed in the genome of the Sardinian Fonni's Dog. Genetics. 2016;204: 737–55. doi: 10.1534/genetics.116.192427 27519604

21. Fogel B. The Encyclopedia of the Dog. New York, NY: DK Publishing, Inc; 1995.

22. Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ. Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaScience. 2015;4. doi: 10.1186/s13742-015-0047-8 25722852

23. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, 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 17701901

24. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics. 2005;21: 263–5. doi: 10.1093/bioinformatics/bth457 15297300

25. Cadieu E, Neff MW, Quignon P, Walsh K, Chase K, Parker HG, et al. Coat variation in the domestic dog is governed by variants in three genes. Science. 2009;326: 150–3. doi: 10.1126/science.1177808 19713490

26. Whitaker DT, Ostrander EA. Hair of the dog: identification of a cis-regulatory module predicted to influence canine coat composition. Genes (Basel). 2019;10. doi: 10.3390/genes10050323 31035530

27. Nuttall T. The genomics revolution: will canine atopic dermatitis be predictable and preventable? Vet Dermatol. 2013;24: 10–8 e3-4. doi: 10.1111/j.1365-3164.2012.01094.x 23331674

28. Merryman-Simpson AE, Wood SH, Fretwell N, Jones PG, McLaren WM, McEwan NA, Clements DN, Carter SD, Ollier WE, Nuttall T. Gene (mRNA) expression in canine atopic dermatitis: microarray analysis. Vet Dermatol. 2008;19: 59–66. doi: 10.1111/j.1365-3164.2008.00653.x 18336422

29. Holm BR, Rest JR, Seewald W. A prospective study of the clinical findings, treatment and histopathology of 44 cases of pyotraumatic dermatitis. Vet Dermatol. 2004;15: 369–76. doi: 10.1111/j.1365-3164.2004.00421.x 15585012

30. Zhao J, Wang B, Yu H, Wang Y, Liu X, Zhang Q. tdrd1 is a germline-specific and sexually dimorphically expressed gene in Paralichthys olivaceus. Gene. 2018;673: 61069.

31. Hales CM, Griner R, Hobdy-Henderson KC, Dorn MC, Hardy D, Kumar R, Navarre J, Chan EK, Lapierre LA, Goldenring JR. Identification and characterization of a family of Rab11-interacting proteins. J Biol Chem. 2001;276: 39067–75. doi: 10.1074/jbc.M104831200 11495908

32. Salmela E, Niskanen J, Arumilli M, Donner J, Lohi H, Hytonen MK. A novel KRT71 variant in curly-coated dogs. Anim Genet. 2019;50: 101–4. doi: 10.1111/age.12746 30456859

33. Bauer A, Hadji Rasouliha S, Brunner MT, Jagannathan V, Bucherm I, Bannoehr J, Varjonen K, Bond R, Bergvall K, Welle MM, Roosje P, Leeb T. A second KRT71 allele in curly-coated dogs. Anim Genet. 2019;50: 97–100. doi: 10.1111/age.12743 30444027

34. Housley DJ, Venta PJ. The long and short of it: evidence that FGF5 is a major determinant of canine 'hair'-itability. Anim Genet. 2006;37: 309–15. doi: 10.1111/j.1365-2052.2006.01448.x 16879338

35. Kirzeder EM, Frank LA, Sowers KD, Rohrbach BW, Donnell RL. Influence of inflammation and coat type on oestrogen receptor immunohistochemistry. Vet Dermatol. 2008;19: 264–70. doi: 10.1111/j.1365-3164.2008.00686.x 18927952

36. Serpell JA, Duffy DL. Dog Breeds And Their Behavior. Horowitz A, editor: Springer-Verlag Publishing; 2014.

37. Hsu Y, Serpell JA. Development and validation of a questionnaire for measuring behavior and temperament traits in pet dogs. J Am Vet Med Assoc. 2003;223: 1293–300. doi: 10.2460/javma.2003.223.1293 14621216

38. Shouldice VL, Edwards AM, Serpell JA, Niel L, Robinson JAB. Expression of behavioural traits in goldenddoles and labradoodles. Animals (Basel). 2019;17. doi: 10.3390/ani9121162 31861203

39. Parada-Bustamante A, Oróstica ML, Reuquen P, Zuñiga LM, Cardenas H, Orihuela PA. The role of mating in oviduct biology. Mol Reprod Dev. 2016;83: 875–83. doi: 10.1002/mrd.22674 27371809

40. Wang J, Fedoseienko A, Chen B, Burstein E, Jia D, Billadeau dD. Endosomal receptor trafficking: Retromer and beyond. Traffic. 2018;19: 578–90. doi: 10.1111/tra.12574 29667289

41. Sahebjada S, Schache M, Richardson AJ, Snibson G, MacGregor S, Daniell M, et al. Evaluating the association between keratoconus and the corneal thickness genes in an independent Australian population. Invest Opthalmol Vis Sci. 2013;17: 8224–8.

42. Rooryck C, VuPhi Y, Souakri N, Burgelin I, Saura R, Lacombe D, et al. Characterization of a de novo balanced translocation t(9,18)(p23;q12.2) in a patient with oculoauriculovertebral spectrum. Eur J Med Genet. 2010;53: 104–7. doi: 10.1016/j.ejmg.2010.01.003 20132917

43. Miller RW. ‘A Frankenstein monster’: Why the Labradoodle creator regrets breeding the dogs. USA Today. 2020 [cited 2020]. Available from:

44. Nicholas FW, Arnott ER, McGreevy PD. Hybrid vigour in dogs? Vet J. 2016;214:77–83. doi: 10.1016/j.tvjl.2016.05.013 27387730

45. Nicholas FW, Wade CM, Williamson P. Disorders in pedigree dogs: Assembling the evidence. The Veterinary Journal. 2010;183: 8–9. doi: 10.1016/j.tvjl.2009.11.008 19963416

46. Abraham G, Inouye M. Fast principal component analysis of large-scale genome-wide data. PLoS One. 2014;9;9(4);e93766. doi: 10.1371/journal.pone.0093766 24718290

47. Alexander DH, Lange K. Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinformatics. 2011;12: 246. doi: 10.1186/1471-2105-12-246 21682921

48. Browning BL, Browning SR. Genotype imputation with millions of reference samples. Am J Hum Genet. 2016;98: 116–26. doi: 10.1016/j.ajhg.2015.11.020 26748515

49. Das S, Forer F, Schönherr S, Sidore C, Locke AE, Kwong A, et al. Next-generation genotype imputation service and methods. Nat Genet. 2016;48: 1284–7. doi: 10.1038/ng.3656 27571263

50. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. The variant call format and VCFtools. Bioinformatics. 2011;27: 2156–8. doi: 10.1093/bioinformatics/btr330 21653522

51. Ripley RD. The R project in statistical computing. Oxford: Oxford University, 2001.

52. Zhang C, Dong SS, Xu JY, He WM, Yang TL. PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics. 2019;15: 1786–8.

Článek vyšel v časopise

PLOS Genetics

2020 Číslo 9

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…

Kurzy Doporučená témata Časopisy
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.


Nemáte účet?  Registrujte se

VIRTUÁLNÍ ČEKÁRNA ČR Jste praktický lékař nebo pediatr? Zapojte se! Jste praktik nebo pediatr? Zapojte se!