Cuba: Exploring the History of Admixture and the Genetic Basis of Pigmentation Using Autosomal and Uniparental Markers

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Cuba is the largest island of the Greater Antilles and its most populous country. The post-Columbian history of the Caribbean has been marked by the encounter of people from different continents. Here, we present an admixture analysis of 1,019 individuals from all the provinces of Cuba, using autosomal, mtDNA and Y-chromosome markers. We also analyzed the association of 16 single nucleotide polymorphisms (SNPs) with quantitative estimates of skin pigmentation (melanin index). The highest proportions of African ancestry were observed in the Southeastern provinces of Santiago de Cuba and Guantánamo, and the highest proportions of Native American ancestry were found in the Eastern provinces of Granma, Holguín and Las Tunas. Similar geographic patterns were observed in the analyses of the uniparental markers. Additionally, by comparing the autosomal and uniparental admixture proportions, we identified a clear sex-biased pattern in the process of gene flow, with a substantially higher European contribution from the paternal side than the maternal side, and conversely higher Native American and African contributions from the maternal side than the paternal side. Finally, we observed that SNPs located in the genes SLC24A5 and SLC45A2 show a strong association with skin pigmentation in the sample.

Vyšlo v časopise: Cuba: Exploring the History of Admixture and the Genetic Basis of Pigmentation Using Autosomal and Uniparental Markers. PLoS Genet 10(7): e32767. doi:10.1371/journal.pgen.1004488
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004488

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Zdroje

1. ViaM, GignouxCR, RothLA, FejermanL, GalanterJ, et al. (2011) History shaped the geographic distribution of genomic admixture on the island of Puerto Rico. PLoS One 6: e16513.

2. TorresJB, StoneAC, KittlesR (2013) An anthropological genetic perspective on creolization in the Anglophone Caribbean. Am J Phys Anthropol 151: 135–143.

3. DeasonML, SalasA, NewmanSP, MacaulayVA, St. A MorrisonEY, et al. (2012) Interdisciplinary approach to the demography of Jamaica. BMC Evol Biol 12: 24.

4. SimmsTM, RodriguezCE, RodriguezR, HerreraRJ (2010) The genetic structure of populations from Haiti and Jamaica reflect divergent demographic histories. Am J Phys Anthropol 142: 49–66.

5. Benn-TorresJ, BonillaC, RobbinsCM, WatermanL, MosesTY, et al. (2008) Admixture and population stratification in African Caribbean populations. Ann Hum Genet 72: 782–790.

6. BrycK, VelezC, KarafetT, Moreno-EstradaA, ReynoldsA, et al. (2010) Colloquium paper: genome-wide patterns of population structure and admixture among Hispanic/Latino populations. Proc Natl Acad Sci USA 107(Suppl 2): 8954–8961.

7. Miljkovic-GacicI, FerrellRE, PatrickAL, KammererCM, BunkerCH (2005) Estimates of African, European and Native American ancestry in Afro-Caribbean men on the island of Tobago. Hum Hered 60: 129–133.

8. CintadoA, CompanioniO, NazabalM, CamachoH, FerrerA, et al. (2009) Admixture estimates for the population of Havana City. Ann Hum Biol 36: 350–360.

9. MendizabalI, SandovalK, Berniell-LeeG, CalafellF, SalasA, et al. (2008) Genetic origin, admixture, and asymmetry in maternal and paternal human lineages in Cuba. BMC Evol Biol 8: 213.

10. Rodríguez SuárezR, ArredondoC, RangelA, MartínezJG, Chinique de ArmasY, et al. (2009) Aportes a la arqueología y la antropología física de Cuba y Las Antillas: sitio arqueológico Canímar Abajo, Matanzas, Cuba. Premio Anual de la Academia de Ciencias de Cuba

11. Lalueza-FoxC, GilbertMTP, Martinez-FuentesAJ, CalafellF, BertranpetitJ (2003) Mitochondrial DNA from Pre-Columbian Ciboneys from Cuba and the prehistoric colonization of the Caribbean. Am J Phys Anthropol 121: 97–108.

12. Guanche J (2011) Componentes étnicos de la nación cubana. La Habana: Editorial Ciencias Sociales.130 p.

13. Le Riverend, J (1967) Historia económica de Cuba.La Habana: Editorial Universitaria. 662 p.

14. Curtin PD (1969) The Atlantic slave trade: a census. Madison: The University of Wisconsin Press. 358 p.

15. Pérez de la Riva, J (1979) El monto de la inmigracion forzada en el siglo XIX. Ciudad de la Habana: Editorial Ciencias Sociales. 47 p.

16. Alfonso León, A (2009) La medición del color de la piel en los censos de población y viviendas. La Habana: Oficina Nacional de Estadísticas. CEPDE.

17. CohenJ (1960) A coefficient of agreement for nominal scales. Educ Phsychol Meas 20: 37–46.

18. CicchettiDV, AllisonT (1971) A new procedure for assessing reliability of scoring EEG sleep recordings. Am J EEG Technol 11: 101–109.

19. FleissJL, CohenJ (1973) The equivalence of weighted kappa and the intraclass correlation coefficient as measures of reliability. Educ Physchol Meas 33: 613–619.

20. ShriverMD, ParraEJ (2000) Comparison of narrow-band reflectance spectroscopy and tristimulus colorimetry for measurements of skin and hair color in persons of different biological ancestry. Am J Phys Anthropol 112: 17–27.

21. KanetskyPA, SwoyerJ, PanossianS, HolmesR, GuerryD, et al. (2002) A polymorphism in the agouti signaling protein gene is associated with human pigmentation. Am J Hum Genet 70: 770–775.

22. BonillaC, BoxillLA, DonaldSA, WilliamsT, SylvesterN, et al. (2005) The 8818G allele of the agouti signaling protein (ASIP) gene is ancestral and is associated with darker skin color in African Americans. Hum Genet 116: 402–406.

23. BelezaS, JohnsonNA, CandilleSI, AbsherDM, CoramMA, et al. (2013) Genetic architecture of skin and eye color in an African-European admixed population. PLoS Genet 9: e1003372.

24. JacobsLC, WollsteinA, LaoO, HofmanA, KlaverCC, et al. (2013) Comprehensive candidate gene study highlights UGT1A and BNC2 as new genes determining continuous skin color variation in Europeans. Hum Genet 132: 147–158.

25. VisserM, KayserM, PalstraRJ (2012) HERC2 rs12913832 modulates human pigmentation by attenuating chromatin-loop formation between a long-range enhancer and the OCA2 promoter. Genome Res 22: 446–455.

26. SturmRA, DuffyDL, ZhaoZZ, LeiteFP, StarkMS, et al. (2008) A single SNP in an evolutionary conserved region within intron 86 of the HERC2 gene determines human blue-brown eye color. Am J Hum Genet 82: 424–431.

27. EibergH, TroelsenJ, NielsenM, MikkelsenA, Mengel-FromJ, et al. (2008) Blue eye color in humans may be caused by a perfectly associated founder mutation in a regulatory element located within the HERC2 gene inhibiting OCA2 expression. Hum Genet 123: 177–187.

28. AmosCI, WangLE, LeeJE, GershenwaldJE, ChenWV, et al. (2011) Genome-wide association study identifies novel loci predisposing to cutaneous melanoma. Hum Mol Genet 20: 5012–5023.

29. BranickiW, BrudnikU, Wojas-PelcA (2009) Interactions between HERC2, OCA2 and MC1R may influence human pigmentation phenotype. Ann Hum Genet 73: 160–170.

30. Ibarrola-VillavaM, FernandezLP, PitaG, BravoJ, FloristanU, et al. (2010) Genetic analysis of three important genes in pigmentation and melanoma susceptibility: CDKN2A, MC1R and HERC2/OCA2. Exp Dermatol 19: 836–844.

31. MillerCT, BelezaS, PollenAA, SchluterD, KittlesRA, et al. (2007) cis-Regulatory changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 131: 1179–1189.

32. SulemP, GudbjartssonDF, StaceySN, HelgasonA, RafnarT, et al. (2007) Genetic determinants of hair, eye and skin pigmentation in Europeans. Nat Genet 39: 1443–1452.

33. NanH, KraftP, HunterDJ, HanJ (2009) Genetic variants in pigmentation genes, pigmentary phenotypes, and risk of skin cancer in Caucasians. Int J Cancer 125: 909–917.

34. LamasonRL, MohideenMA, MestJR, WongAC, NortonHL, et al. (2005) SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science 310: 1782–1786.

35. NortonHL, KittlesRA, ParraE, McKeigueP, MaoX, et al. (2007) Genetic evidence for the convergent evolution of light skin in Europeans and East Asians. Mol Biol Evol 24: 710–722.

36. ShriverMD, ParraEJ, DiosS, BonillaC, NortonH, et al. (2003) Skin pigmentation, biogeographical ancestry and admixture mapping. Hum Genet 112: 387–399.

37. BelezaS, SantosAM, McEvoyB, AlvesI, MartinhoC, et al. (2013) The timing of pigmentation lightening in Europeans. Mol Biol Evol 30: 24–35.

38. DevlinB (1999) RoederK (1999) Genomic control for association studies. Biometrics 55: 997–1004.

39. Oficina Nacional de Estadísticas (2006) Informe Nacional Censo de Población y Viviendas Cuba-2002. La Habana: Oficina Nacional de Estadísticas.

40. Pérez De La Riva J (2004) La conquista del espacio cubano. La Habana. Editado por: Fundación Fernando Ortíz. 243 p.

41. Dacal-Moure R, Rivero de la Calle M (1997) Art and archaeology of pre-columbian Cuba. University of Pittsburgh Press. 160 p.

42. Pérez Jr., LA (2006) Cuba: Between reform and revolution, 3rdedition. New York: Oxford University Press. 539 p.

43. De la Sagra, R (1842) Historia física, política y natural de la isla de Cuba. París, t. 1, p. 144.

44. Moreno-EstradaA, GravelS, ZakhariaF, McCauleyJL, ByrnesJK, et al. (2013) Reconstructing the population genetic history of the Caribbean. PLoS Genet 9: e1003925.

45. GalanterJM, Fernández-LopezJC, GignouxCR, Barnholtz-SloanJ, Fernández-RozadillaC, et al. (2012) Development of a panel of genome-wide ancestry informative markers to study admixture throughout the Americas. PLoS Genet 8: e1002554.

46. Álvarez-IglesiasV, Mosquera-MiguelA, CerezoM, QuintánsB, ZarrabeitiaMT, et al. (2009) New population and phylogenetic features of the internal variation within mitochondrial DNA macro-haplogroup R0. PLoS One 4: e5112.

47. Álvarez-IglesiasV, JaimeJC, CarracedoA, SalasA (2007) Coding region mitochondrial DNA SNPs: targeting East Asian and Native American haplogroups. Forensic Sci Int Genet 1: 44–55.

48. BandeltH-J, van OvenM, SalasA (2012) Haplogrouping mitochondrial DNA sequences in Legal Medicine/Forensic Genetics. Int J Legal Med 126: 901–916.

49. van OvenM, KayserM (2009) Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation. Hum Mutat 30: 386–394.

50. AndrewsRM, KubackaI, ChinneryPF, LightowlersRN, TurnbullDM, et al. (1999) Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat Genet 23: 147.

51. SalasA, CobleM, DesmyterS, GrzybowskiT, GusmãoL, et al. (2012) A cautionary note on switching mitochondrial DNA reference sequences in forensic genetics. Forensic Sci Int Genet 6: e182–e184.

52. SalasA, CarracedoA, MacaulayV, RichardsM, BandeltH-J (2005) A practical guide to mitochondrial DNA error prevention in clinical, forensic, and population genetics. Biochem Biophys Res Commun 335: 891–899.

53. BriónM, SanchezJJ, BaloghK, ThackerC, Blanco-VereaA, et al. (2005) Introduction of a single nucleodite polymorphism-based “Major Y-chromosome haplogroup typing kit” suitable for predicting the geographical origin of male lineages. Electrophoresis 26: 4411–4420.

54. Blanco-VereaA, JaimeJC, BriónM, CarracedoA (2010) Y-chromosome lineages in native South American population. Forensic Sci Int Genet 4: 187–193.

55. HoggartCJ, ParraEJ, ShriverMD, BonillaC, KittlesRA, et al. (2003) Control of confounding of genetic associations in stratified populations. Am J Hum Genet 72: 1492–1504.

56. HoggartCJ, ShriverMD, KittlesRA, ClaytonDG, McKeiguePM (2004) Design and analysis of admixture mapping studies. Am J Hum Genet 74: 965–978.