#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

True Colors: Commercially-acquired morphological genotypes reveal hidden allele variation among dog breeds, informing both trait ancestry and breed potential


Autoři: Dayna L. Dreger aff001;  Blair N. Hooser aff001;  Angela M. Hughes aff002;  Balasubramanian Ganesan aff002;  Jonas Donner aff003;  Heidi Anderson aff003;  Lauren Holtvoigt aff002;  Kari J. Ekenstedt aff001
Působiště autorů: Department of Basic Medical Sciences, College of Veterinary Medicine, Purdue University, West Lafayette, IN, United States of America aff001;  Wisdom Health, Vancouver, WA, United States of America aff002;  Wisdom Health, Helsinki, Finland aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223995

Souhrn

Direct-to-consumer canine genetic testing is becoming increasingly popular among dog owners. The data collected therein provides intriguing insight into the current status of morphological variation present within purebred populations. Mars WISDOM PANELTM data from 11,790 anonymized dogs, representing 212 breeds and 4 wild canine species, were evaluated at genes associated with 7 coat color traits and 5 physical characteristics. Frequencies for all tested alleles at these 12 genes were determined by breed and by phylogenetic grouping. A sub-set of the data, consisting of 30 breeds, was divided into separate same-breed populations based on country of collection, body size, coat variation, or lineages selected for working or conformation traits. Significantly different (p ≤ 0.00167) allele frequencies were observed between populations for at least one of the tested genes in 26 of the 30 breeds. Next, standard breed descriptions from major American and international registries were used to determine colors and tail lengths (e.g. genetic bobtail) accepted within each breed. Alleles capable of producing traits incongruous with breed descriptions were observed in 143 breeds, such that random mating within breeds has probabilities of between 4.9e-7 and 0.25 of creating undesirable phenotypes. Finally, the presence of rare alleles within breeds, such as those for the recessive black coloration and natural bobtail, was combined with previously published identity-by-decent haplotype sharing levels to propose pathways by which the alleles may have spread throughout dog breeds. Taken together, this work demonstrates that: 1) the occurrence of low frequency alleles within breeds can reveal the influence of regional or functional selection practices; 2) it is possible to visualize the potential historic connections between breeds that share rare alleles; and 3) the necessity of addressing conflicting ideals in breed descriptions relative to actual genetic potential is crucial.

Klíčová slova:

Haplotypes – Phenotypes – Alleles – Pets and companion animals – Dogs – Phylogeography – Variant genotypes – Ears


Zdroje

1. The American Kennel Club. The Complete Dog Book. New York: Ballantine Books; 2006.

2. Little CC. The inheritance of coat color in dogs. Ithaca, New York: Comstock Publishing Associates; 1957.

3. Kerns JA, Newton J, Berryere TG, Rubin EM, Cheng JF, Schmutz SM, et al. Characterization of the dog Agouti gene and a nonagouti mutation in German Shepherd Dogs. Mamm Genome. 2004;15(10):798–808. doi: 10.1007/s00335-004-2377-1 15520882

4. Berryere TG, Kerns JA, Barsh GS, Schmutz SM. Association of an Agouti allele with fawn or sable coat color in domestic dogs. Mamm Genome. 2005;16(4):262–72. doi: 10.1007/s00335-004-2445-6 15965787

5. Dreger DL, Schmutz SM. A SINE insertion causes the black-and-tan and saddle tan phenotypes in domestic dogs. J Hered. 2011;102 Suppl.

6. Schmutz SM, Berryere TG, Ellinwood NM, Kerns JA, Barsh GS. MCIR Studies in Dogs with Melanistic Mask or Brindle Patterns. J Hered. 2003;94(1):69–73. doi: 10.1093/jhered/esg014 12692165

7. Dreger DL, Schmutz SM. A new mutation in MC1R explains a coat color phenotype in 2 “old” breeds: Saluki and Afghan Hound. J Hered. 2010;101(5):644–9. doi: 10.1093/jhered/esq061 20525767

8. Newton JM, Wilkie AL, He L, Jordan SA, Metallinos DL, Holmes NG, et al. Melanocortin 1 receptor variation in the domestic dog. Mamm Genome. 2000;11(1):24–30. doi: 10.1007/s003350010005 10602988

9. Candille SI, Kaelin CB, Cattanach BM, Yu B, Thompson DA, Nix MA, et al. A beta-defensin mutation causes black coat color in domestic dogs. Science. 2007;318(5855):1418–23. doi: 10.1126/science.1147880 17947548

10. Kerns JA, Cargill EJ, Clark LA, Candille SI, Berryere TG, Olivier M, et al. Linkage and segregation analysis of black and brindle coat color in domestic dogs. Genetics. 2007;176(3):1679–89. doi: 10.1534/genetics.107.074237 17483404

11. Schmutz SM, Berryere TG, Goldfinch AD. TYRP1 and MC1R genotypes and their effects on coat color in dogs. Mamm Genome. 2002;13(7):380–7. doi: 10.1007/s00335-001-2147-2 12140685

12. Hrckova Turnova E, Majchrakova Z, Bielikova M, Soltys K, Turna J, Dudas A. A novel mutation in the TYRP1 gene associated with brown coat colour in the Australian Shepherd Dog Breed. Anim Genet. 2017;48(5):626.

13. Jancuskova T, Langevin M, Pekova S. TYRP1: c.555T>G is a recurrent mutation found in Australian Shepherd and Miniature American Shepherd dogs. Anim Genet. 2018;500–1. doi: 10.1111/age.12709 30109695

14. Clark LA, Tsai KL, Starr AN, Nowend KL, Murphy KE. A missense mutation in the 20S proteasome β2 subunit of Great Danes having harlequin coat patterning. Genomics. 2011;97(4):244–8. doi: 10.1016/j.ygeno.2011.01.003 21256207

15. Clark LA, Wahl JM, Rees CA, Murphy KE. Retrotransposon insertion in SILV is responsible for merle patterning of the domestic dog. Proc Natl Acad Sci. 2006;103(5):1376–81. doi: 10.1073/pnas.0506940103 16407134

16. Murphy SC, Evans JM, Tsai KL, Clark LA. Length variations within the Merle retrotransposon of canine PMEL: Correlating genotype with phenotype. Mob DNA. Mobile DNA; 2018;9(1):1–11.

17. Karlsson EK, Baranowska I, Wade CM, Salmon Hillbertz NHC, Zody MC, Anderson N, et al. Efficient mapping of mendelian traits in dogs through genome-wide association. Nat Genet. 2007;39(11):1321–8. doi: 10.1038/ng.2007.10 17906626

18. Schmutz SM, Berryere TG, Dreger DL. MITF and white spotting in dogs: A population study. J Hered. 2009;100(Suppl 1):S66–74.

19. Dreger DL, Parker HG, Ostrander EA, Schmutz SM. Identification of a mutation that is associated with the saddle tan and black-and-tan phenotypes in Basset Hounds and Pembroke Welsh Corgis. J Hered. 2013;104(3):399–406. doi: 10.1093/jhered/est012 23519866

20. 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(5949):150–3. doi: 10.1126/science.1177808 19713490

21. Parker HG, Chase K, Cadieu E, Lark KG, Ostrander EA. An insertion in the RSPO2 gene correlates with improper coat in the Portuguese water dog. J Hered. 2010;101(5):612–7. doi: 10.1093/jhered/esq068 20562213

22. Bauer A, Hadji Rasouliha S, Brunner MT, Jagannathan V, Bucher I, Bannoehr J, et al. A second KRT71 allele in curly coated dogs. Anim Genet. 2018;2016–9.

23. Salmela E, Niskanen J, Arumilli M, Donner J, Lohi H, Hytönen MK. A novel KRT71 variant in curly-coated dogs. Anim Genet. 2018;50:101–4. doi: 10.1111/age.12746 30456859

24. Dierks C, Mömke S, Philipp U, Distl O. Allelic heterogeneity of FGF5 mutations causes the long-hair phenotype in dogs. Anim Genet. 2013;44(4):425–31. doi: 10.1111/age.12010 23384345

25. Haworth K, Putt W, Cattanach B, Breen M, Binns M, Lingaas F, et al. Canine homolog of the T-box transcription factor T; failure of the protein to bind to its DNA target leads to a short-tail phenotype. Mamm Genome. 2001;12(3):212–8. doi: 10.1007/s003350010253 11252170

26. Hytönen MK, Grall A, Hédan B, Dréano S, Seguin SJ, Delattre D, et al. Ancestral T-box mutation is present in many, but not all, short-tailed dog breeds. J Hered. 2009;100(2):236–40. doi: 10.1093/jhered/esn085 18854372

27. Vaysse A, Ratnakumar A, Derrien T, Axelsson E, Pielberg GR, Sigurdsson S, et al. Identification of genomic regions associated with phenotypic variation between dog breeds using selection mapping. PLoS Genet. 2011 Oct 13;7(10):e1002316. doi: 10.1371/journal.pgen.1002316 22022279

28. 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(1):1489. doi: 10.1038/s41467-019-09373-w 30940804

29. Schoenebeck JJ, Hutchinson SA, Byers A, Beale HC, Carrington B, Faden DL, et al. Variation of BMP3 Contributes to Dog Breed Skull Diversity. PLoS Genet. 2012;8(8):1–11.

30. Marchant TW, Johnson EJ, McTeir L, Johnson CI, Gow A, Liuti T, et al. Canine Brachycephaly Is Associated with a Retrotransposon-Mediated Missplicing of SMOC2. Curr Biol. 2017;27(11):1573–1584.e6. doi: 10.1016/j.cub.2017.04.057 28552356

31. Faculty of Veterinary Science University of Sydney. Online Mendelian Inheritance in Animals, OMIA [Internet]. [cited 2019 Jan 14]. Available from: http://omia.angis.org.au/

32. 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(4):697–708. doi: 10.1016/j.celrep.2017.03.079 28445722

33. Talenti A, Dreger DL, Frattini S, Polli M, Marelli S, Harris AC, et al. Studies of modern Italian dog populations reveal multiple patterns for domestic breed evolution. Ecol Evol. 2017;8:2911–25.

34. Eckardt J, Kluth S, Dierks C, Philipp U, Distl O. Population screening for the mutation associated with osteogenesis imperfecta in dachshunds. Vet Rec. 2013;172(14):364. doi: 10.1136/vr.101122 23315765

35. Holder AL, Price JA, Adams JP, Volk HA, Catchpole B. A retrospective study of the prevalence of the canine degenerative myelopathy associated superoxide dismutase 1 mutation (SOD1:c.118G > A) in a referral population of German Shepherd dogs from the UK. Canine Genet Epidemiol. 2014;1(1):10.

36. Monobe M, Bulla C, da Silva R, Lunsford K, Araujo JP Jr. Frequency of the MDR1 mutant allele associated with multidrug sensitivity in dogs from Brazil. Vet Med Res Reports. 2015;(January):111.

37. Mizukami K, Yabuki A, Kohyama M, Kushida K, Rahman MM, Uddin MM, et al. Molecular prevalence of multiple genetic disorders in Border collies in Japan and recommendations for genetic counselling. Vet J. 2016;214:21–3. doi: 10.1016/j.tvjl.2016.05.004 27387721

38. Takanosu M. Different allelic frequency of progressive rod-cone degeneration in two populations of Labrador Retrievers in Japan. J Vet Med Sci. 2017;79(10):1746–8. doi: 10.1292/jvms.17-0243 28855430

39. Crespi JA, Barrientos LS, Giovambattista G. von Willebrand disease type 1 in Doberman Pinscher dogs: genotyping and prevalence of the mutation in the Buenos Aires region, Argentina. J Vet Diagnostic Investig. 2018;30(2):310–4.

40. Ahonen S, Seath I, Rusbridge C, Holt S, Key G, Wang T, et al. Nationwide genetic testing towards eliminating Lafora disease from Miniature Wirehaired Dachshunds in the United Kingdom. Canine Genet Epidemiol. Canine Genetics and Epidemiology; 2018;5(1):2.

41. Donner J, Anderson H, Davison S, Hughes AM, Bouirmane J, Lindqvist J, et al. Frequency and distribution of 152 genetic disease variants in over 100,000 mixed breed and purebred dogs. PLOS Genet. 2018;14(4):1–20.

42. Pearson D. The Bedlington Terrier [Internet]. Ashcroft Bedlington Terriers. 2015 [cited 2019 Aug 8]. Available from: http://www.ashcrofterriers.com/about-bedlington-terriers

43. Lhasa Apso [Internet]. Dog Breed Info Center. 2018 [cited 2019 Apr 30]. Available from: https://www.dogbreedinfo.com/lhasaapso.htm

44. Think my new sheltie is docked [Internet]. Sheltie Nation. 2011 [cited 2019 Apr 30]. Available from: https://sheltieforums.com/threads/think-my-new-sheltie-is-docked.10163/

45. Short stumpy tail [Internet]. Staffordshire bull terrier. 2011 [cited 2019 Apr 30]. Available from: http://staffy-bull-terrier.niceboard.com/t10059-short-stumpy-tail

46. Opinions on having tail docked [Internet]. r/vizsla. 2017 [cited 2019 Apr 30]. Available from: https://www.reddit.com/r/vizsla/comments/6ksvt6/opinions_on_having_tail_docked/

47. Dumont BL, Payseur BA. Evolution of the genomic rate of recombination in mammals. Evolution (N Y). 2008;62(2):276–94.

48. Oguro-Okano M, Honda M, Yamazaki K, Okano K. Mutations in the Melanocortin 1 Receptor, β-Defensin103 and Agouti Signaling Protein Genes, and Their Association with Coat Color Phenotypes in Akita-Inu Dogs. J Vet Med Sci. 2011;73(7):853–8. doi: 10.1292/jvms.10-0439 21321476

49. Schmutz SM, Berryere TG, Barta JL, Reddick KD, Schmutz JK. Agouti sequence polymorphisms in coyotes, wolves and dogs suggest hybridization. J Hered. 2007;98(4):351–5. doi: 10.1093/jhered/esm036 17630272

50. Brockerville RM, McGrath MJ, Pilgrim BL, Marshall HD. Sequence analysis of three pigmentation genes in the Newfoundland population of Canis latrans links the Golden Retriever Mc1r variant to white coat color in coyotes. Mamm Genome. 2013;24(3–4):134–41. doi: 10.1007/s00335-012-9443-x 23297074

51. Schweizer RM, Durvasula A, Smith J, Vohr SH, Stahler DR, Galaverni M, et al. Natural selection and origin of a melanistic allele in North American Gray Wolves. Mol Biol Evol. 2018;35(5):1190–209. doi: 10.1093/molbev/msy031 29688543

52. Boyko AR, Quignon P, Li L, Schoenebeck JJ, Degenhardt JD, Lohmueller KE, et al. A simple genetic architecture underlies morphological variation in dogs. PLoS Biol. 2010;8(8):49–50.

53. Pilot M, Greco C, VonHoldt BM, Jędrzejewski W, Sidorovich VE, Konopinski MK, et al. Widespread, long-term admixture between grey wolves and domestic dogs across Eurasia and its implications for the conservation status of hybrids. Evol Appl. 2018;(July 2017):662–80. doi: 10.1111/eva.12595 29875809

54. Dufresnes C, Remollino N, Stoffel C, Manz R, Weber J, Fumagalli L. Two decades of non-invasive genetic monitoring of the grey wolves recolonizing the Alps support very limited dog introgression. 2019;(November 2018):1–9.

55. Croxton-Smith A, editor. Hounds and Dogs, their care, training & working for hunting, shooting, coursing, hawking, police purposes. London: Lonsdale Library; 1932. doi: 10.3390/ani9070390

56. Lee RB. A history and description of the modern dogs of Great Britain and Ireland: Sporting Division. London: Horace Cox; 1897.

57. Graham JA. The Sporting Dog. New York: The MacMillan Company; 1904.

58. Smith S, editor. The encyclopedia of North American sporting dogs: Written by Sportsmen for Sportmen. 1st ed. Minocqua, WI: Willow Creek Press; 2002.

59. Campbell KL, Campbell JR. Companion Animals: Their biology, care, health and management. 2nd ed. Upper Saddle River, NJ: Pearson Prentice Hall; 2009.

60. Quignon P, Herbin L, Cadieu E, Kirkness EF, Hédan B, Mosher DS, et al. Canine Population Structure: Assessment and Impact of Intra-Breed Stratification on SNP-Based Association Studies. PLoS One. 2007 Dec 19;2(12):e1324-. doi: 10.1371/journal.pone.0001324 18091995

61. Shearin AL, Hedan B, Cadieu E, Erich SA, Schmidt EV., Faden DL, et al. The MTAP-CDKN2A locus confers susceptibility to a naturally occurring canine cancer. Cancer Epidemiol Biomarkers Prev. 2012;21(7):1019–27. doi: 10.1158/1055-9965.EPI-12-0190-T 22623710

62. Edwards SM, Woolliams JA, Hickey JM, Blott SC, Clements DN, Sánchez-Molano E, et al. Joint genomic prediction of canine hip dysplasia in UK and US labrador retrievers. Front Genet. 2018;9(March):1–12.

63. Pedersen NC, Liu H, McLaughlin B, Sacks BN. Genetic characterization of healthy and sebaceous adenitis affected Standard Poodles from the United States and United Kingdom. Tissue Antigens. 2012;80:46–57. doi: 10.1111/j.1399-0039.2012.01876.x 22512808

64. Sinmez CC, Yigit A, Aslim G. Tail docking and ear cropping in dogs: a short review of laws and welfare aspects in the Europe and Turkey. Ital J Anim Sci. 2017;16(3):431–7.

65. South African Veterinary Council. The South African Veterinary Council policy on tail docking in dogs [Internet]. 2008 [cited 2019 Jan 14]. Available from: https://www.savc.org.za/tail-docking

66. New Zealand Veterinary Association. Canine Tail Docking [Internet]. 2018 [cited 2019 Jan 14]. Available from: https://www.nzva.org.nz/page/policytaildock

67. Australian Veterinary Association. AVA welcomes end to tail docking in Western Australia [Internet]. 2010. Available from: https://www.ava.com.au/mediarelease/ava-welcomes-end-tail-docking-western-australia

68. Animal Welfare Veterinary Division. Information on dog tail docking provided for the Animal Welfare Division [Internet]. 2002. Available from: https://web.archive.org/web/20070626075746/http://www.defra.gov.uk/animalh/welfare/domestic/awbillconsulttaildocking.pdf

69. Wijnrocx K, Francois L, Stinckens A, Janssens S, Buys N. Half of 23 Belgian dog breeds has a compromised genetic diversity, as revealed by genealogical and molecular data analysis. J Anim Breed Genet. 2016;133:375–83. doi: 10.1111/jbg.12203 26927793

70. Pedersen NC, Pooch AS, Liu H. A genetic assessment of the English bulldog. Canine Genet Epidemiol. Canine Genetics and Epidemiology; 2016;3(1):6.

71. Kettunen A, Daverdin M, Helfjord T, Berg P. Cross-breeding is inevitable to conserve the highly inbred population of puffin hunter: The Norwegian Lundehund. PLoS One. 2017;12(1):1–16.

72. Wiener P, Sánchez-Molano E, Clements DN, Woolliams JA, Haskell MJ, Blott SC. Genomic data illuminates demography, genetic structure and selection of a popular dog breed. BMC Genomics. 2017;18(1):609. doi: 10.1186/s12864-017-3933-x 28806925

73. Mastrangelo S, Filippo B, Auzino B, Marco R, Spaterna A, Ciampolini R. Genome-wide diversity and runs of homozygosity in the “Braque Français, type Pyrénées” dog breed. BMC Res Notes. 2018;11(1):11–6. doi: 10.1186/s13104-017-3119-2

74. Pohjoismäki JLO, Lampi S, Donner J, Anderson H. Origins and wanderings of the finnish hunting spitzes. PLoS One. 2018;13(6):1–17.

75. Jansson M, Laikre L. Pedigree data indicate rapid inbreeding and loss of genetic diversity within populations of native, traditional dog breeds of conservation concern. PLoS One. 2018;13(9):1–17.

76. 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 Dec 1;9(12):1445–60. doi: 10.1242/dmm.027037 27874836

77. Ostrander EA, Kruglyak L. Unleashing the Canine Genome Unleashing the Canine Genome. Genome Res. 2000;10:1271–4. doi: 10.1101/gr.155900 10984444

78. Donner J, Kaukonen M, Anderson H, Möller F, Kyöstilä K, Sankari S, et al. Genetic panel screening of nearly 100 mutations reveals new insights into the breed distribution of risk variants for canine hereditary disorders. PLoS One. 2016;11(8):1–18.

79. Venables WN, Ripley BD. Modern Applied Statistics with S. 4th ed. New York: Springer; 2002.

80. R Core Team. R: A language and environment for statistical computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2017. Available from: https://www.r-project.org.


Článok vyšiel v časopise

PLOS One


2019 Číslo 10
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#