Skin colour: A window into human phenotypic evolution and environmental adaptation.

environmental adaptation modern humans molecular evolution skin colour

Journal

Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478

Informations de publication

Date de publication:
07 May 2024
Historique:
revised: 13 04 2024
received: 31 01 2024
accepted: 17 04 2024
medline: 7 5 2024
pubmed: 7 5 2024
entrez: 7 5 2024
Statut: aheadofprint

Résumé

As modern humans ventured out of Africa and dispersed around the world, they faced novel environmental challenges that led to geographic adaptations including skin colour. Over the long history of human evolution, skin colour has changed dramatically, showing tremendous diversity across different geographical regions, for example, the majority of individuals from the expansive lands of Africa have darker skin, whereas the majority of people from Eurasia exhibit lighter skin. What adaptations did lighter skin confer upon modern humans as they migrated from Africa to Eurasia? What genetic mechanisms underlie the diversity of skin colour observed in different populations? In recent years, scientists have gradually gained a deeper understanding of the interactions between pigmentation gene and skin colour through population-based genomic studies of different groups around the world, particularly in East Asia and Africa. In this review, we summarize our current understanding of 26 skin colour-related pigmentation genes and 48 SNPs that influence skin colour. Important pigmentation genes across three major populations are described in detail: MFSD12, SLC24A5, PDPK1 and DDB1/CYB561A3/TMEM138 influence skin colour in African populations; OCA2, KITLG, SLC24A2, GNPAT and PAH are key to the evolution of skin pigmentation in East Asian populations; and SLC24A5, SLC45A2, TYR, TYRP1, ASIP, MC1R and IRF4 significantly contribute to the lightening of skin colour in European populations. We summarized recent findings in genomic studies of skin colour in populations that implicate diverse geographic environments, local adaptation among populations, gene flow and multi-gene interactions as factors influencing skin colour diversity.

Identifiants

pubmed: 38713101
doi: 10.1111/mec.17369
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

e17369

Subventions

Organisme : National Natural Science Foundation of China
ID : 32070579
Organisme : National Natural Science Foundation of China
ID : 32370664
Organisme : Natural Science Foundation of Henan Province
ID : 222300420067

Informations de copyright

© 2024 John Wiley & Sons Ltd.

Références

Abdel‐Malek, Z., Suzuki, I., Tada, A., Im, S., & Akcali, C. (1999). The melanocortin‐1 receptor and human pigmentation. Annals of the New York Academy of Sciences, 885, 117–133. https://doi.org/10.1111/j.1749‐6632.1999.tb08669.x
Adelmann, C. H., Traunbauer, A. K., Chen, B., Condon, K. J., Chan, S. H., Kunchok, T., Lewis, C. A., & Sabatini, D. M. (2020). MFSD12 mediates the import of cysteine into melanosomes and lysosomes. Nature, 588(7839), 699–704. https://doi.org/10.1038/s41586‐020‐2937‐x
Adhikari, K., Mendoza‐Revilla, J., Sohail, A., Fuentes‐Guajardo, M., Lampert, J., Chacón‐Duque, J. C., Hurtado, M., Villegas, V., Granja, V., Acuña‐Alonzo, V., Jaramillo, C., Arias, W., Lozano, R. B., Everardo, P., Gómez‐Valdés, J., Villamil‐Ramírez, H., Silva de Cerqueira, C. C., Hunemeier, T., Ramallo, V., … Ruiz‐Linares, A. (2019). A GWAS in Latin Americans highlights the convergent evolution of lighter skin pigmentation in Eurasia. Nature Communications, 10(1), 358. https://doi.org/10.1038/s41467‐018‐08147‐0
Alkan, C., Coe, B. P., & Eichler, E. E. (2011). Genome structural variation discovery and genotyping. Nature Reviews Genetics, 12(5), 363–376. https://doi.org/10.1038/nrg2958
Anello, M., Daverio, M. S., Silbestro, M. B., Vidal‐Rioja, L., & Di Rocco, F. (2019). Characterization and expression analysis of KIT and MITF‐M genes in llamas and their relation to white coat color. Animal Genetics, 50(2), 143–149. https://doi.org/10.1111/age.12769
Arnold, M., Singh, D., Laversanne, M., Vignat, J., Vaccarella, S., Meheus, F., Cust, A. E., de Vries, E., Whiteman, D. C., & Bray, F. (2022). Global burden of cutaneous melanoma in 2020 and projections to 2040. JAMA Dermatology, 158(5), 495–503. https://doi.org/10.1001/jamadermatol.2022.0160
Bae, C. J., Douka, K., & Petraglia, M. D. (2017). On the origin of modern humans: Asian perspectives. Science, 358(6368). https://doi.org/10.1126/science.aai9067
Bajpai, V. K., Swigut, T., Mohammed, J., Naqvi, S., Arreola, M., Tycko, J., Kim, T. C., Pritchard, J. K., Bassik, M. C., & Wysocka, J. (2023). A genome‐wide genetic screen uncovers determinants of human pigmentation. Science, 381(6658), eade6289. https://doi.org/10.1126/science.ade6289
Batai, K., Cui, Z., Arora, A., Shah‐Williams, E., Hernandez, W., Ruden, M., Hollowell, C. M. P., Hooker, S. E., Bathina, M., Murphy, A. B., Bonilla, C., & Kittles, R. A. (2021). Genetic loci associated with skin pigmentation in African Americans and their effects on vitamin D deficiency. PLoS Genetics, 17(2), e1009319. https://doi.org/10.1371/journal.pgen.1009319
Beirl, A. J., Linbo, T. H., Cobb, M. J., & Cooper, C. D. (2014). oca2 regulation of chromatophore differentiation and number is cell type specific in zebrafish. Pigment Cell & Melanoma Research, 27(2), 178–189. https://doi.org/10.1111/pcmr.12205
Beleza, S., Santos, A. M., McEvoy, B., Alves, I., Martinho, C., Cameron, E., Shriver, M. D., Parra, E. J., & Rocha, J. (2013). The timing of pigmentation lightening in Europeans. Molecular Biology and Evolution, 30(1), 24–35. https://doi.org/10.1093/molbev/mss207
Beyer, R. M., Krapp, M., Eriksson, A., & Manica, A. (2021). Climatic windows for human migration out of Africa in the past 300,000 years. Nature Communications, 12(1), 4889. https://doi.org/10.1038/s41467‐021‐24779‐1
Bobe, R., & Wood, B. (2022). Estimating origination times from the early hominin fossil record. Evolutionary Anthropology, 31(2), 92–102. https://doi.org/10.1002/evan.21928
Bouillon, R., & Antonio, L. (2020). Nutritional rickets: Historic overview and plan for worldwide eradication. The Journal of Steroid Biochemistry and Molecular Biology, 198, 105563. https://doi.org/10.1016/j.jsbmb.2019.105563
Bower, C., & Stanley, F. J. (1989). Dietary folate as a risk factor for neural‐tube defects: Evidence from a case‐control study in Western Australia. The Medical Journal of Australia, 150(11), 613–619. https://doi.org/10.5694/j.1326‐5377.1989.tb136723.x
Branda, R. F., & Eaton, J. W. (1978). Skin color and nutrient photolysis: An evolutionary hypothesis. Science, 201(4356), 625–626. https://doi.org/10.1126/science.675247
Brenner, M., & Hearing, V. J. (2008). The protective role of melanin against UV damage in human skin. Photochemistry and Photobiology, 84(3), 539–549. https://doi.org/10.1111/j.1751‐1097.2007.00226.x
Brilliant, M. H. (2001). The mouse p (pink‐eyed dilution) and human P genes, oculocutaneous albinism type 2 (OCA2), and melanosomal pH. Pigment Cell Research, 14(2), 86–93. https://doi.org/10.1034/j.1600‐0749.2001.140203.x
Cal, L., Suarez‐Bregua, P., Cerdá‐Reverter, J. M., Braasch, I., & Rotllant, J. (2017). Fish pigmentation and the melanocortin system. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 211, 26–33. https://doi.org/10.1016/j.cbpa.2017.06.001
Cal, L., Suarez‐Bregua, P., Comesaña, P., Owen, J., Braasch, I., Kelsh, R., Cerdá‐Reverter, J. M., & Rotllant, J. (2019). Countershading in zebrafish results from an Asip1 controlled dorsoventral gradient of pigment cell differentiation. Scientific Reports, 9(1), 3449. https://doi.org/10.1038/s41598‐019‐40251‐z
Candille, S. I., Absher, D. M., Beleza, S., Bauchet, M., McEvoy, B., Garrison, N. A., Li, J. Z., Myers, R. M., Barsh, G. S., Tang, H., & Shriver, M. D. (2012). Genome‐wide association studies of quantitatively measured skin, hair, and eye pigmentation in four European populations. PLoS One, 7(10), e48294. https://doi.org/10.1371/journal.pone.0048294
Cook, A. L., Chen, W., Thurber, A. E., Smit, D. J., Smith, A. G., Bladen, T. G., Brown, D. L., Duffy, D. L., Pastorino, L., Bianchi‐Scarra, G., Helen Leonard, J., Stow, J. L., & Sturm, R. A. (2009). Analysis of cultured human melanocytes based on polymorphisms within the SLC45A2/MATP, SLC24A5/NCKX5, and OCA2/P loci. The Journal of Investigative Dermatology, 129(2), 392–405. https://doi.org/10.1038/jid.2008.211
Cooper, C. D. (2017). Insights from zebrafish on human pigment cell disease and treatment. Developmental Dynamics, 246(11), 889–896. https://doi.org/10.1002/dvdy.24550
Crawford, N. G., Kelly, D. E., Hansen, M. E. B., Beltrame, M. H., Fan, S., Bowman, S. L., Jewett, E., Ranciaro, A., Thompson, S., Lo, Y., Pfeifer, S. P., Jensen, J. D., Campbell, M. C., Beggs, W., Hormozdiari, F., Mpoloka, S. W., Mokone, G. G., Nyambo, T., Meskel, D. W., … Tishkoff, S. A. (2017). Loci associated with skin pigmentation identified in African populations. Science, 358(6365). https://doi.org/10.1126/science.aan8433
Cuomo, O., Gala, R., Pignataro, G., Boscia, F., Secondo, A., Scorziello, A., Pannaccione, A., Viggiano, D., Adornetto, A., Molinaro, P., Li, X. F., Lytton, J., di Renzo, G., & Annunziato, L. (2008). A critical role for the potassium‐dependent sodium‐calcium exchanger NCKX2 in protection against focal ischemic brain damage. The Journal of Neuroscience, 28(9), 2053–2063. https://doi.org/10.1523/jneurosci.4912‐07.2008
Cuomo, O., Sirabella, R., Boscia, F., Casamassa, A., Lytton, J., Annunziato, L., & Pignataro, G. (2022). K(+)‐dependent Na(+)/Ca(2+) exchanger isoform 2, Nckx2, takes part in the neuroprotection elicited by ischemic preconditioning in brain ischemia. International Journal of Molecular Sciences, 23(13). https://doi.org/10.3390/ijms23137128
Del Bino, S., Ito, S., Sok, J., Nakanishi, Y., Bastien, P., Wakamatsu, K., & Bernerd, F. (2015). Chemical analysis of constitutive pigmentation of human epidermis reveals constant eumelanin to pheomelanin ratio. Pigment Cell & Melanoma Research, 28(6), 707–717. https://doi.org/10.1111/pcmr.12410
d'Ischia, M., Wakamatsu, K., Napolitano, A., Briganti, S., Garcia‐Borron, J. C., Kovacs, D., Meredith, P., Pezzella, A., Picardo, M., Sarna, T., Simon, J. D., & Ito, S. (2013). Melanins and melanogenesis: Methods, standards, protocols. Pigment Cell & Melanoma Research, 26(5), 616–633. https://doi.org/10.1111/pcmr.12121
Donnelly, M. P., Paschou, P., Grigorenko, E., Gurwitz, D., Barta, C., Lu, R. B., Zhukova, O. V., Kim, J. J., Siniscalco, M., New, M., Li, H., Kajuna, S. L. B., Manolopoulos, V. G., Speed, W. C., Pakstis, A. J., Kidd, J. R., & Kidd, K. K. (2012). A global view of the OCA2‐HERC2 region and pigmentation. Human Genetics, 131(5), 683–696. https://doi.org/10.1007/s00439‐011‐1110‐x
Dooley, C. M., Schwarz, H., Mueller, K. P., Mongera, A., Konantz, M., Neuhauss, S. C., Nüsslein‐Volhard, C., & Geisler, R. (2013). Slc45a2 and V‐ATPase are regulators of melanosomal pH homeostasis in zebrafish, providing a mechanism for human pigment evolution and disease. Pigment Cell & Melanoma Research, 26(2), 205–217. https://doi.org/10.1111/pcmr.12053
D'Orazio, J., Jarrett, S., Amaro‐Ortiz, A., & Scott, T. (2013). UV radiation and the skin. International Journal of Molecular Sciences, 14(6), 12222–12248. https://doi.org/10.3390/ijms140612222
Du, Z., Huang, K., Zhao, J., Song, X., Xing, X., Wu, Q., Zhang, L., & Xu, C. (2017). Comparative transcriptome analysis of raccoon dog skin to determine melanin content in hair and melanin distribution in skin. Scientific Reports, 7, 40903. https://doi.org/10.1038/srep40903
Duffy, D. L., Montgomery, G. W., Chen, W., Zhao, Z. Z., le, L., James, M. R., Hayward, N. K., Martin, N. G., & Sturm, R. A. (2007). A three‐single‐nucleotide polymorphism haplotype in intron 1 of OCA2 explains most human eye‐color variation. American Journal of Human Genetics, 80(2), 241–252. https://doi.org/10.1086/510885
Duffy, D. L., Zhao, Z. Z., Sturm, R. A., Hayward, N. K., Martin, N. G., & Montgomery, G. W. (2010). Multiple pigmentation gene polymorphisms account for a substantial proportion of risk of cutaneous malignant melanoma. The Journal of Investigative Dermatology, 130(2), 520–528. https://doi.org/10.1038/jid.2009.258
Eckhardt, R. B. (2021). Human mitochondrial DNA diversity is compatible with the multiregional continuity theory of the origin of Homo sapiens. Anthropological Review, 84, 487–502. https://doi.org/10.2478/anre‐2021‐0032
Edwards, M., Bigham, A., Tan, J., Li, S., Gozdzik, A., Ross, K., & Parra, E. J. (2010). Association of the OCA2 polymorphism His615Arg with melanin content in east Asian populations: Further evidence of convergent evolution of skin pigmentation. PLoS Genetics, 6(3), e1000867. https://doi.org/10.1371/journal.pgen.1000867
Eiberg, H., Troelsen, J., Nielsen, M., Mikkelsen, A., Mengel‐From, J., Kjaer, K. W., & Hansen, L. (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. Human Genetics, 123(2), 177–187. https://doi.org/10.1007/s00439‐007‐0460‐x
Fan, S., Spence, J. P., Feng, Y., Hansen, M. E. B., Terhorst, J., Beltrame, M. H., Ranciaro, A., Hirbo, J., Beggs, W., Thomas, N., Nyambo, T., Mpoloka, S. W., Mokone, G. G., Njamnshi, A. K., Fokunang, C., Meskel, D. W., Belay, G., Song, Y. S., & Tishkoff, S. A. (2023). Whole‐genome sequencing reveals a complex African population demographic history and signatures of local adaptation. Cell, 186(5), 923–939.e914. https://doi.org/10.1016/j.cell.2023.01.042
Feng, Y., Xie, N., Inoue, F., Fan, S., Saskin, J., Zhang, C., Zhang, F., Hansen, M. E. B., Nyambo, T., Mpoloka, S. W., Mokone, G. G., Fokunang, C., Belay, G., Njamnshi, A. K., Marks, M. S., Oancea, E., Ahituv, N., & Tishkoff, S. A. (2024). Integrative functional genomic analyses identify genetic variants influencing skin pigmentation in Africans. Nature Genetics, 56, 258–272. https://doi.org/10.1038/s41588‐023‐01626‐1
Fitzpatrick, T. B., Becker, S. W., Jr., Lerner, A. B., & Montgomery, H. (1950). Tyrosinase in human skin: Demonstration of its presence and of its role in human melanin formation. Science, 112(2904), 223–225. https://doi.org/10.1126/science.112.2904.223
Galway‐Witham, J., & Stringer, C. (2018). How did Homo sapiens evolve? Science, 360(6395), 1296–1298. https://doi.org/10.1126/science.aat6659
García‐Borrón, J. C., Abdel‐Malek, Z., & Jiménez‐Cervantes, C. (2014). MC1R, the cAMP pathway, and the response to solar UV: Extending the horizon beyond pigmentation. Pigment Cell & Melanoma Research, 27(5), 699–720. https://doi.org/10.1111/pcmr.12257
Ginger, R. S., Askew, S. E., Ogborne, R. M., Wilson, S., Ferdinando, D., Dadd, T., Smith, A. M., Kazi, S., Szerencsei, R. T., Winkfein, R. J., Schnetkamp, P. P. M., & Green, M. R. (2008). SLC24A5 encodes a trans‐Golgi network protein with potassium‐dependent sodium‐calcium exchange activity that regulates human epidermal melanogenesis. The Journal of Biological Chemistry, 283(9), 5486–5495. https://doi.org/10.1074/jbc.M707521200
Graf, J., Hodgson, R., & van Daal, A. (2005). Single nucleotide polymorphisms in the MATP gene are associated with normal human pigmentation variation. Human Mutation, 25(3), 278–284. https://doi.org/10.1002/humu.20143
Graf, J., Voisey, J., Hughes, I., & van Daal, A. (2007). Promoter polymorphisms in the MATP (SLC45A2) gene are associated with normal human skin color variation. Human Mutation, 28(7), 710–717. https://doi.org/10.1002/humu.20504
Grollemund, R., Branford, S., Bostoen, K., Meade, A., Venditti, C., & Pagel, M. (2015). Bantu expansion shows that habitat alters the route and pace of human dispersals. Proceedings of the National Academy of Sciences of the United States of America, 112(43), 13296–13301. https://doi.org/10.1073/pnas.1503793112
Grønskov, K., Ek, J., & Brondum‐Nielsen, K. (2007). Oculocutaneous albinism. Orphanet Journal of Rare Diseases, 2, 43. https://doi.org/10.1186/1750‐1172‐2‐43
Guernsey, M. W., Ritscher, L., Miller, M. A., Smith, D. A., Schöneberg, T., & Shapiro, M. D. (2013). A Val85Met mutation in melanocortin‐1 receptor is associated with reductions in eumelanic pigmentation and cell surface expression in domestic rock pigeons (Columba livia). PLoS One, 8(8), e74475. https://doi.org/10.1371/journal.pone.0074475
Günther, T., Malmström, H., Svensson, E. M., Omrak, A., Sánchez‐Quinto, F., Kılınç, G. M., Krzewińska, M., Eriksson, G., Fraser, M., Edlund, H., Munters, A. R., Coutinho, A., Simões, L. G., Vicente, M., Sjölander, A., Jansen Sellevold, B., Jørgensen, R., Claes, P., Shriver, M. D., … Jakobsson, M. (2018). Population genomics of Mesolithic Scandinavia: Investigating early postglacial migration routes and high‐latitude adaptation. PLoS Biology, 16(1), e2003703. https://doi.org/10.1371/journal.pbio.2003703
Guo, Y., Rubin, C. J., Rönneburg, T., Wang, S., Li, H., Hu, X., & Carlborg, Ö. (2024). Whole‐genome selective sweep analyses identifies the region and candidate gene associated with white earlobe color in Mediterranean chickens. Poultry Science, 103(1), 103232. https://doi.org/10.1016/j.psj.2023.103232
Guyonneau, L., Murisier, F., Rossier, A., Moulin, A., & Beermann, F. (2004). Melanocytes and pigmentation are affected in dopachrome tautomerase knockout mice. Molecular and Cellular Biology, 24(8), 3396–3403. https://doi.org/10.1128/mcb.24.8.3396‐3403.2004
Han, J., Kraft, P., Nan, H., Guo, Q., Chen, C., Qureshi, A., Hankinson, S. E., Hu, F. B., Duffy, D. L., Zhao, Z. Z., Martin, N. G., Montgomery, G. W., Hayward, N. K., Thomas, G., Hoover, R. N., Chanock, S., & Hunter, D. J. (2008). A genome‐wide association study identifies novel alleles associated with hair color and skin pigmentation. PLoS Genetics, 4(5), e1000074. https://doi.org/10.1371/journal.pgen.1000074
Hanel, A., & Carlberg, C. (2020a). Skin colour and vitamin D: An update. Experimental Dermatology, 29(9), 864–875. https://doi.org/10.1111/exd.14142
Hanel, A., & Carlberg, C. (2020b). Vitamin D and evolution: Pharmacologic implications. Biochemical Pharmacology, 173, 113595. https://doi.org/10.1016/j.bcp.2019.07.024
Harding, R. M., Healy, E., Ray, A. J., Ellis, N. S., Flanagan, N., Todd, C., Dixon, C., Sajantila, A., Jackson, I. J., Birch‐Machin, M. A., & Rees, J. L. (2000). Evidence for variable selective pressures at MC1R. American Journal of Human Genetics, 66(4), 1351–1361. https://doi.org/10.1086/302863
Harris, M. L., Baxter, L. L., Loftus, S. K., & Pavan, W. J. (2010). Sox proteins in melanocyte development and melanoma. Pigment Cell & Melanoma Research, 23(4), 496–513. https://doi.org/10.1111/j.1755‐148X.2010.00711.x
Hartman, M. L., & Czyz, M. (2015). MITF in melanoma: Mechanisms behind its expression and activity. Cellular and Molecular Life Sciences, 72(7), 1249–1260. https://doi.org/10.1007/s00018‐014‐1791‐0
Hearing, V. J. (2011). Determination of melanin synthetic pathways. The Journal of Investigative Dermatology, 131(E1), E8–e11. https://doi.org/10.1038/skinbio.2011.4
Henn, B. M., Gignoux, C., Lin, A. A., Oefner, P. J., Shen, P., Scozzari, R., Cruciani, F., Tishkoff, S. A., Mountain, J. L., & Underhill, P. A. (2008). Y‐chromosomal evidence of a pastoralist migration through Tanzania to southern Africa. Proceedings of the National Academy of Sciences of the United States of America, 105(31), 10693–10698. https://doi.org/10.1073/pnas.0801184105
Holick, M. F. (2017). The vitamin D deficiency pandemic: Approaches for diagnosis, treatment and prevention. Reviews in Endocrine & Metabolic Disorders, 18(2), 153–165. https://doi.org/10.1007/s11154‐017‐9424‐1
Howe, K., Clark, M. D., Torroja, C. F., Torrance, J., Berthelot, C., Muffato, M., Collins, J. E., Humphray, S., McLaren, K., Matthews, L., McLaren, S., Sealy, I., Caccamo, M., Churcher, C., Scott, C., Barrett, J. C., Koch, R., Rauch, G. J., White, S., … Stemple, D. L. (2013). The zebrafish reference genome sequence and its relationship to the human genome. Nature, 496(7446), 498–503. https://doi.org/10.1038/nature12111
Ibarrola‐Villava, M., Hu, H. H., Guedj, M., Fernandez, L. P., Descamps, V., Basset‐Seguin, N., Bagot, M., Benssussan, A., Saiag, P., Fargnoli, M. C., Peris, K., Aviles, J. A., Lluch, A., Ribas, G., & Soufir, N. (2012). MC1R, SLC45A2 and TYR genetic variants involved in melanoma susceptibility in southern European populations: Results from a meta‐analysis. European Journal of Cancer, 48(14), 2183–2191. https://doi.org/10.1016/j.ejca.2012.03.006
Iovine, B., Iannella, M. L., & Bevilacqua, M. A. (2011). Damage‐specific DNA binding protein 1 (DDB1): A protein with a wide range of functions. The International Journal of Biochemistry & Cell Biology, 43(12), 1664–1667. https://doi.org/10.1016/j.biocel.2011.09.001
Ishengoma, E. (2023). Vertebrate genomics and adaptation ‐ status and prospects in Africa. Molecular Ecology, 32(13), 3368–3381. https://doi.org/10.1111/mec.16936
Ito, S., & Wakamatsu, K. (2008). Chemistry of mixed melanogenesis‐pivotal roles of dopaquinone. Photochemistry and Photobiology, 84(3), 582–592. https://doi.org/10.1111/j.1751‐1097.2007.00238.x
Jablonski, N. G. (2021). The evolution of human skin pigmentation involved the interactions of genetic, environmental, and cultural variables. Pigment Cell & Melanoma Research, 34(4), 707–729. https://doi.org/10.1111/pcmr.12976
Jablonski, N. G., & Chaplin, G. (2000). The evolution of human skin coloration. Journal of Human Evolution, 39(1), 57–106. https://doi.org/10.1006/jhev.2000.0403
Jablonski, N. G., & Chaplin, G. (2010). Colloquium paper: Human skin pigmentation as an adaptation to UV radiation. Proceedings of the National Academy of Sciences of the United States of America, 107(Suppl 2), 8962–8968. https://doi.org/10.1073/pnas.0914628107
Jacobs, L. C., Hamer, M. A., Gunn, D. A., Deelen, J., Lall, J. S., van Heemst, D., Uh, H. W., Hofman, A., Uitterlinden, A. G., Griffiths, C. E. M., Beekman, M., Slagboom, P. E., Kayser, M., Liu, F., & Nijsten, T. (2015). A genome‐wide association study identifies the skin color genes IRF4, MC1R, ASIP, and BNC2 influencing facial pigmented spots. The Journal of Investigative Dermatology, 135(7), 1735–1742. https://doi.org/10.1038/jid.2015.62
Jacobs, L. C., Wollstein, A., Lao, O., Hofman, A., Klaver, C. C., Uitterlinden, A. G., Nijsten, T., Kayser, M., & Liu, F. (2013). Comprehensive candidate gene study highlights UGT1A and BNC2 as new genes determining continuous skin color variation in Europeans. Human Genetics, 132(2), 147–158. https://doi.org/10.1007/s00439‐012‐1232‐9
Jones, P., Lucock, M., Veysey, M., & Beckett, E. (2018). The vitamin D−Folate hypothesis as an evolutionary model for skin pigmentation: An update and integration of current ideas. Nutrients, 10(5). https://doi.org/10.3390/nu10050554
Ju, D., & Mathieson, I. (2021). The evolution of skin pigmentation‐associated variation in West Eurasia. Proceedings of the National Academy of Sciences of the United States of America, 118(1). https://doi.org/10.1073/pnas.2009227118
Kadekaro, A. L., Leachman, S., Kavanagh, R. J., Swope, V., Cassidy, P., Supp, D., Sartor, M., Schwemberger, S., Babcock, G., Wakamatsu, K., Ito, S., Koshoffer, A., Boissy, R. E., Manga, P., Sturm, R. A., & Abdel‐Malek, Z. A. (2010). Melanocortin 1 receptor genotype: An important determinant of the damage response of melanocytes to ultraviolet radiation. The FASEB Journal, 24(10), 3850–3860. https://doi.org/10.1096/fj.10‐158485
Kayser, M., Branicki, W., Parson, W., & Phillips, C. (2023). Recent advances in forensic DNA phenotyping of appearance, ancestry and age. Forensic Science International: Genetics, 65, 102870. https://doi.org/10.1016/j.fsigen.2023.102870
Kelsh, R. N., Sosa, K. C., Owen, J. P., & Yates, C. A. (2017). Zebrafish adult pigment stem cells are multipotent and form pigment cells by a progressive fate restriction process: Clonal analysis identifies shared origin of all pigment cell types. BioEssays, 39(3). https://doi.org/10.1002/bies.201600234
Kinjo, T. G., Szerencsei, R. T., Winkfein, R. J., Kang, K., & Schnetkamp, P. P. (2003). Topology of the retinal cone NCKX2 Na/Ca‐K exchanger. Biochemistry, 42(8), 2485–2491. https://doi.org/10.1021/bi0270788
Kirschbaum, F. (1975). Investigations on the colour pattern of the zebra fishBrachydanio rerio (Cyprinidae, teleostei). Wilehm Roux's Archives of Developmental Biology, 177(2), 129–152. https://doi.org/10.1007/bf00848526
Klungland, H., Våge, D. I., Gomez‐Raya, L., Adalsteinsson, S., & Lien, S. (1995). The role of melanocyte‐stimulating hormone (MSH) receptor in bovine coat color determination. Mammalian Genome, 6(9), 636–639. https://doi.org/10.1007/bf00352371
Kobayashi, T., & Hearing, V. J. (2007). Direct interaction of tyrosinase with Tyrp1 to form heterodimeric complexes in vivo. Journal of Cell Science, 120(Pt 24), 4261–4268. https://doi.org/10.1242/jcs.017913
Kratochwil, C. F., Urban, S., & Meyer, A. (2019). Genome of the Malawi golden cichlid fish (Melanochromis auratus) reveals exon loss of oca2 in an amelanistic morph. Pigment Cell & Melanoma Research, 32(5), 719–723. https://doi.org/10.1111/pcmr.12799
Lamason, R. L., Mohideen, M. A., Mest, J. R., Wong, A. C., Norton, H. L., Aros, M. C., Jurynec, M. J., Mao, X., Humphreville, V. R., Humbert, J. E., Sinha, S., Moore, J. L., Jagadeeswaran, P., Zhao, W., Ning, G., Makalowska, I., McKeigue, P. M., O'Donnell, D., Kittles, R., … Cheng, K. C. (2005). SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science, 310(5755), 1782–1786. https://doi.org/10.1126/science.1116238
Lasisi, T., & Shriver, M. D. (2018). Focus on African diversity confirms complexity of skin pigmentation genetics. Genome Biology, 19(1), 13. https://doi.org/10.1186/s13059‐018‐1395‐3
Le, L., Escobar, I. E., Ho, T., Lefkovith, A. J., Latteri, E., Haltaufderhyde, K. D., Dennis, M. K., Plowright, L., Sviderskaya, E. V., Bennett, D. C., Oancea, E., & Marks, M. S. (2020). SLC45A2 protein stability and regulation of melanosome pH determine melanocyte pigmentation. Molecular Biology of the Cell, 31(24), 2687–2702. https://doi.org/10.1091/mbc.E20‐03‐0200
Levy, C., Khaled, M., & Fisher, D. E. (2006). MITF: Master regulator of melanocyte development and melanoma oncogene. Trends in Molecular Medicine, 12(9), 406–414. https://doi.org/10.1016/j.molmed.2006.07.008
Li, J., Wang, Q. E., Zhu, Q., El‐Mahdy, M. A., Wani, G., Praetorius‐Ibba, M., & Wani, A. A. (2006). DNA damage binding protein component DDB1 participates in nucleotide excision repair through DDB2 DNA‐binding and cullin 4A ubiquitin ligase activity. Cancer Research, 66(17), 8590–8597. https://doi.org/10.1158/0008‐5472.Can‐06‐1115
Li, Y. X., Zhang, X. H., Pang, Y. Z., Qi, Y. X., & Zhao, S. J. (2019). Construction of MC1R and ASIP eukaryotic expression vector and its regulation of plumage color in Japanese quail (Coturnix japonica). The Journal of Poultry Science, 56(2), 84–90. https://doi.org/10.2141/jpsa.0180058
Lin, J. Y., & Fisher, D. E. (2007). Melanocyte biology and skin pigmentation. Nature, 445(7130), 843–850. https://doi.org/10.1038/nature05660
Lin, M., Siford, R. L., Martin, A. R., Nakagome, S., Möller, M., Hoal, E. G., Bustamante, C. D., Gignoux, C. R., & Henn, B. M. (2018). Rapid evolution of a skin‐lightening allele in southern African KhoeSan. Proceedings of the National Academy of Sciences of the United States of America, 115(52), 13324–13329. https://doi.org/10.1073/pnas.1801948115
Liu, F., Visser, M., Duffy, D. L., Hysi, P. G., Jacobs, L. C., Lao, O., Zhong, K., Walsh, S., Chaitanya, L., Wollstein, A., Zhu, G., Montgomery, G. W., Henders, A. K., Mangino, M., Glass, D., Bataille, V., Sturm, R. A., Rivadeneira, F., Hofman, A., … Kayser, M. (2015). Genetics of skin color variation in Europeans: Genome‐wide association studies with functional follow‐up. Human Genetics, 134(8), 823–835. https://doi.org/10.1007/s00439‐015‐1559‐0
Liu, H., Wang, J., Hu, J., Wang, L., Guo, Z., Fan, W., Xu, Y., Liu, D., Zhang, Y., Xie, M., Tang, J., Huang, W., Zhang, Q., Zhou, Z., & Hou, S. (2022). Genome‐wide association analysis reveal the genetic reasons affect melanin spot accumulation in beak skin of ducks. BMC Genomics, 23(1), 236. https://doi.org/10.1186/s12864‐022‐08444‐5
Liu, X., Zhou, R., Peng, Y., Zhang, C., Li, L., Lu, C., & Li, X. (2019). Feather follicles transcriptome profiles in Bashang long‐tailed chickens with different plumage colors. Genes & Genomics, 41(11), 1357–1367. https://doi.org/10.1007/s13258‐018‐0740‐y
Liu, Y., Mao, X., Krause, J., & Fu, Q. (2021). Insights into human history from the first decade of ancient human genomics. Science, 373(6562), 1479–1484. https://doi.org/10.1126/science.abi8202
Loftus, S. K., Lundh, L., Watkins‐Chow, D. E., Baxter, L. L., Pairo‐Castineira, E., NISC Comparative Sequencing Program, Jackson, I. J., Oetting, W. S., Pavan, W. J., & Adams, D. R. (2021). A custom capture sequence approach for oculocutaneous albinism identifies structural variant alleles at the OCA2 locus. Human Mutation, 42(10), 1239–1253. https://doi.org/10.1002/humu.24257
Mack, M., Kowalski, E., Grahn, R., Bras, D., Penedo, M. C. T., & Bellone, R. (2017). Two variants in SLC24A5 are associated with "Tiger‐eye" iris pigmentation in Puerto Rican Paso Fino horses. G3 (Bethesda), 7(8), 2799–2806. https://doi.org/10.1534/g3.117.043786
Makova, K., & Norton, H. (2005). Worldwide polymorphism at the MC1R locus and normal pigmentation variation in humans. Peptides, 26(10), 1901–1908. https://doi.org/10.1016/j.peptides.2004.12.032
Maresca, V., Flori, E., Briganti, S., Mastrofrancesco, A., Fabbri, C., Mileo, A. M., Paggi, M. G., & Picardo, M. (2008). Correlation between melanogenic and catalase activity in in vitro human melanocytes: A synergic strategy against oxidative stress. Pigment Cell & Melanoma Research, 21(2), 200–205. https://doi.org/10.1111/j.1755‐148X.2007.00432.x
Martin, A. R., Lin, M., Granka, J. M., Myrick, J. W., Liu, X., Sockell, A., Atkinson, E. G., Werely, C. J., Möller, M., Sandhu, M. S., Kingsley, D. M., Hoal, E. G., Liu, X., Daly, M. J., Feldman, M. W., Gignoux, C. R., Bustamante, C. D., & Henn, B. M. (2017). An unexpectedly complex architecture for skin pigmentation in Africans. Cell, 171(6), 1340–1353.e1314. https://doi.org/10.1016/j.cell.2017.11.015
McGuire, J. (1965). Melanin granule dispersion in epidermal melanocytes. The Journal of Investigative Dermatology, 45(6), 547–548. https://doi.org/10.1038/jid.1965.171
Miller, C. T., Beleza, S., Pollen, A. A., Schluter, D., Kittles, R. A., Shriver, M. D., & Kingsley, D. M. (2007). Cis‐regulatory changes in kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell, 131(6), 1179–1189. https://doi.org/10.1016/j.cell.2007.10.055
Miyamura, Y., Coelho, S. G., Schlenz, K., Batzer, J., Smuda, C., Choi, W., Brenner, M., Passeron, T., Zhang, G., Kolbe, L., Wolber, R., & Hearing, V. J. (2011). The deceptive nature of UVA tanning versus the modest protective effects of UVB tanning on human skin. Pigment Cell & Melanoma Research, 24(1), 136–147. https://doi.org/10.1111/j.1755‐148X.2010.00764.x
Mosca, S., & Morrone, A. (2023). Human skin pigmentation: From a biological feature to a social determinant. Healthcare (Basel), 11(14). https://doi.org/10.3390/healthcare11142091
Mun, Y., Kim, W., & Shin, D. (2023). Melanocortin 1 receptor (MC1R): Pharmacological and therapeutic aspects. International Journal of Molecular Sciences, 24(15). https://doi.org/10.3390/ijms241512152
Mundy, N. I. (2005). A window on the genetics of evolution: MC1R and plumage colouration in birds. Proceedings of the Biological Sciences, 272(1573), 1633–1640. https://doi.org/10.1098/rspb.2005.3107
Nan, H., Kraft, P., Qureshi, A. A., Guo, Q., Chen, C., Hankinson, S. E., Hu, F. B., Thomas, G., Hoover, R. N., Chanock, S., Hunter, D. J., & Han, J. (2009). Genome‐wide association study of tanning phenotype in a population of European ancestry. The Journal of Investigative Dermatology, 129(9), 2250–2257. https://doi.org/10.1038/jid.2009.62
Nasti, T. H., & Timares, L. (2015). MC1R, eumelanin and pheomelanin: Their role in determining the susceptibility to skin cancer. Photochemistry and Photobiology, 91(1), 188–200. https://doi.org/10.1111/php.12335
Norton, H. L., Kittles, R. A., Parra, E., McKeigue, P., Mao, X., Cheng, K., Canfield, V. A., Bradley, D. G., McEvoy, B., & Shriver, M. D. (2007). Genetic evidence for the convergent evolution of light skin in Europeans and east Asians. Molecular Biology and Evolution, 24(3), 710–722. https://doi.org/10.1093/molbev/msl203
Nowacka‐Woszuk, J., Salamon, S., Gorna, A., & Switonski, M. (2013). Missense polymorphisms in the MC1R gene of the dog, red fox, arctic fox and Chinese raccoon dog. Journal of Animal Breeding and Genetics, 130(2), 136–141. https://doi.org/10.1111/jbg.12005
O'Rourke, D. H., & Raff, J. A. (2010). The human genetic history of the Americas: The final frontier. Current Biology, 20(4), R202–R207. https://doi.org/10.1016/j.cub.2009.11.051
Park, S., Morya, V. K., Nguyen, D. H., Singh, B. K., Lee, H. B., & Kim, E. K. (2015). Unrevealing the role of P‐protein on melanosome biology and structure, using siRNA‐mediated down regulation of OCA2. Molecular and Cellular Biochemistry, 403(1–2), 61–71. https://doi.org/10.1007/s11010‐015‐2337‐y
Patterson, L. B., & Parichy, D. M. (2019). Zebrafish pigment pattern formation: Insights into the development and evolution of adult form. Annual Review of Genetics, 53, 505–530. https://doi.org/10.1146/annurev‐genet‐112618‐043741
Pavan, W. J., & Sturm, R. A. (2019). The genetics of human skin and hair pigmentation. Annual Review of Genomics and Human Genetics, 20, 41–72. https://doi.org/10.1146/annurev‐genom‐083118‐015230
Pavel, S. (1993). Dynamics of melanogenesis intermediates. The Journal of Investigative Dermatology, 100(2 Suppl), 162s–165s.
Peng, Y., Yang, Z., Zhang, H., Cui, C., Qi, X., Luo, X., Tao, X., Wu, T., Ouzhuluobu, Basang, Ciwangsangbu, Danzengduojie, Chen, H., Shi, H., & Su, B. (2011). Genetic variations in Tibetan populations and high‐altitude adaptation at the Himalayas. Molecular Biology and Evolution, 28(2), 1075–1081. https://doi.org/10.1093/molbev/msq290
Pickrell, J. K., Patterson, N., Loh, P. R., Lipson, M., Berger, B., Stoneking, M., Pakendorf, B., & Reich, D. (2014). Ancient west Eurasian ancestry in southern and eastern Africa. Proceedings of the National Academy of Sciences of the United States of America, 111(7), 2632–2637. https://doi.org/10.1073/pnas.1313787111
Praetorius, C., Grill, C., Stacey, S. N., Metcalf, A. M., Gorkin, D. U., Robinson, K. C., van Otterloo, E., Kim, R. S. Q., Bergsteinsdottir, K., Ogmundsdottir, M. H., Magnusdottir, E., Mishra, P. J., Davis, S. R., Guo, T., Zaidi, M. R., Helgason, A. S., Sigurdsson, M. I., Meltzer, P. S., Merlino, G., … Steingrimsson, E. (2013). A polymorphism in IRF4 affects human pigmentation through a tyrosinase‐dependent MITF/TFAP2A pathway. Cell, 155(5), 1022–1033. https://doi.org/10.1016/j.cell.2013.10.022
Protas, M. E., Hersey, C., Kochanek, D., Zhou, Y., Wilkens, H., Jeffery, W. R., Zon, L. I., Borowsky, R., & Tabin, C. J. (2006). Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nature Genetics, 38(1), 107–111. https://doi.org/10.1038/ng1700
Pu, Y., Pu, S., Chen, Y., Kong, Q., Liu, X., Zhao, Q., Xu, K., Liu, J., Li, M., Xu, X., Qiao, X., Su, B., Chen, J., & Yang, Z. (2024). Weakened tanning ability is an important mechanism for evolutionary skin lightening in east Asians. Journal of Genetics and Genomics. https://doi.org/10.1016/j.jgg.2024.03.001
Quillen, E. E., Norton, H. L., Parra, E. J., Lona‐Durazo, F., Ang, K. C., Illiescu, F. M., Pearson, L. N., Shriver, M. D., Lasisi, T., Gokcumen, O., Starr, I., Lin, Y. L., Martin, A. R., & Jablonski, N. G. (2019). Shades of complexity: New perspectives on the evolution and genetic architecture of human skin. American Journal of Physical Anthropology, 168(Suppl 67), 4–26. https://doi.org/10.1002/ajpa.23737
Quillen, E. E., & Shriver, M. D. (2011). Unpacking human evolution to find the genetic determinants of human skin pigmentation. The Journal of Investigative Dermatology, 131(E1), E5–E7. https://doi.org/10.1038/skinbio.2011.3
Rana, B. K., Hewett‐Emmett, D., Jin, L., Chang, B. H., Sambuughin, N., Lin, M., Watkins, S., Bamshad, M., Jorde, L. B., Ramsay, M., Jenkins, T., & Li, W. H. (1999). High polymorphism at the human melanocortin 1 receptor locus. Genetics, 151(4), 1547–1557. https://doi.org/10.1093/genetics/151.4.1547
Read, A. P., & Newton, V. E. (1997). Waardenburg syndrome. Journal of Medical Genetics, 34(8), 656–665. https://doi.org/10.1136/jmg.34.8.656
Relethford, J. H. (1997). Hemispheric difference in human skin color. American Journal of Physical Anthropology, 104(4), 449–457. https://doi.org/10.1002/(sici)1096‐8644(199712)104:4<449::Aid‐ajpa2>3.0.Co;2‐n
Rezvani, H. R., Cario‐André, M., Pain, C., Ged, C., deVerneuil, H., & Taïeb, A. (2007). Protection of normal human reconstructed epidermis from UV by catalase overexpression. Cancer Gene Therapy, 14(2), 174–186. https://doi.org/10.1038/sj.cgt.7701000
Richardson, J., Lundegaard, P. R., Reynolds, N. L., Dorin, J. R., Porteous, D. J., Jackson, I. J., & Patton, E. E. (2008). mc1r pathway regulation of zebrafish melanosome dispersion. Zebrafish, 5(4), 289–295. https://doi.org/10.1089/zeb.2008.0541
Rinchik, E. M., Bultman, S. J., Horsthemke, B., Lee, S. T., Strunk, K. M., Spritz, R. A., Avidano, K. M., Jong, M. T. C., & Nicholls, R. D. (1993). A gene for the mouse pink‐eyed dilution locus and for human type II oculocutaneous albinism. Nature, 361(6407), 72–76. https://doi.org/10.1038/361072a0
Roulin, A., & Ducrest, A. L. (2013). Genetics of colouration in birds. Seminars in Cell & Developmental Biology, 24(6–7), 594–608. https://doi.org/10.1016/j.semcdb.2013.05.005
Saenko, S. V., Lamichhaney, S., Martinez Barrio, A., Rafati, N., Andersson, L., & Milinkovitch, M. C. (2015). Amelanism in the corn snake is associated with the insertion of an LTR‐retrotransposon in the OCA2 gene. Scientific Reports, 5, 17118. https://doi.org/10.1038/srep17118
Saito, T., Okamura, K., Kosaki, R., Wakamatsu, K., Ito, S., Nakajima, O., Yamashita, H., Hozumi, Y., & Suzuki, T. (2022). Impact of a SLC24A5 variant on the retinal pigment epithelium of a Japanese patient with oculocutaneous albinism type 6. Pigment Cell & Melanoma Research, 35(2), 212–219. https://doi.org/10.1111/pcmr.13024
Schallreuter, K. U., & Wood, J. M. (1999). The importance of L‐phenylalanine transport and its autocrine turnover to L‐tyrosine for melanogenesis in human epidermal melanocytes. Biochemical and Biophysical Research Communications, 262(2), 423–428. https://doi.org/10.1006/bbrc.1999.1241
Schlebusch, C. M., Malmström, H., Günther, T., Sjödin, P., Coutinho, A., Edlund, H., Munters, A. R., Vicente, M., Steyn, M., Soodyall, H., Lombard, M., & Jakobsson, M. (2017). Southern African ancient genomes estimate modern human divergence to 350,000 to 260,000 years ago. Science, 358(6363), 652–655. https://doi.org/10.1126/science.aao6266
Scortegagna, M., Ruller, C., Feng, Y., Lazova, R., Kluger, H., Li, J. L., de, S. K., Rickert, R., Pellecchia, M., Bosenberg, M., & Ronai, Z. A. (2014). Genetic inactivation or pharmacological inhibition of Pdk1 delays development and inhibits metastasis of Braf(V600E)::Pten(−/−) melanoma. Oncogene, 33(34), 4330–4339. https://doi.org/10.1038/onc.2013.383
Shibukawa, Y., Kang, K. J., Kinjo, T. G., Szerencsei, R. T., Altimimi, H. F., Pratikhya, P., Winkfein, R. J., & Schnetkamp, P. P. M. (2007). Structure‐function relationships of the NCKX2 Na+/Ca2+‐K+ exchanger. Annals of the New York Academy of Sciences, 1099, 16–28. https://doi.org/10.1196/annals.1387.054
Shriver, M. D., Parra, E. J., Dios, S., Bonilla, C., Norton, H., Jovel, C., Pfaff, C., Jones, C., Massac, A., Cameron, N., Baron, A., Jackson, T., Argyropoulos, G., Jin, L., Hoggart, C. J., McKeigue, P. M., & Kittles, R. A. (2003). Skin pigmentation, biogeographical ancestry and admixture mapping. Human Genetics, 112(4), 387–399. https://doi.org/10.1007/s00439‐002‐0896‐y
Simonson, T. S., Yang, Y., Huff, C. D., Yun, H., Qin, G., Witherspoon, D. J., Bai, Z., Lorenzo, F. R., Xing, J., Jorde, L. B., Prchal, J. T., & Ge, R. L. (2010). Genetic evidence for high‐altitude adaptation in Tibet. Science, 329(5987), 72–75. https://doi.org/10.1126/science.1189406
Sinha, R. P., & Häder, D. P. (2002). UV‐induced DNA damage and repair: A review. Photochemical & Photobiological Sciences, 1(4), 225–236. https://doi.org/10.1039/b201230h
Smit, A. K., Collazo‐Roman, M., Vadaparampil, S. T., Valavanis, S., del Rio, J., Soto, B., Flores, I., Dutil, J., & Kanetsky, P. A. (2020). MC1R variants and associations with pigmentation characteristics and genetic ancestry in a Hispanic, predominately Puerto Rican, population. Scientific Reports, 10(1), 7303. https://doi.org/10.1038/s41598‐020‐64019‐y
Smith, R., Healy, E., Siddiqui, S., Flanagan, N., Steijlen, P. M., Rosdahl, I., Jacques, J. P., Rogers, S., Turner, R., Jackson, I. J., Birch‐Machin, M. A., & Rees, J. L. (1998). Melanocortin 1 receptor variants in an Irish population. The Journal of Investigative Dermatology, 111(1), 119–122. https://doi.org/10.1046/j.1523‐1747.1998.00252.x
Soejima, M., & Koda, Y. (2007). Population differences of two coding SNPs in pigmentation‐related genes SLC24A5 and SLC45A2. International Journal of Legal Medicine, 121(1), 36–39. https://doi.org/10.1007/s00414‐006‐0112‐z
Soejima, M., Tachida, H., Ishida, T., Sano, A., & Koda, Y. (2006). Evidence for recent positive selection at the human AIM1 locus in a European population. Molecular Biology and Evolution, 23(1), 179–188. https://doi.org/10.1093/molbev/msj018
Stanisz, H., Stark, A., Kilch, T., Schwarz, E. C., Müller, C. S., Peinelt, C., Hoth, M., Niemeyer, B. A., Vogt, T., & Bogeski, I. (2012). ORAI1 Ca(2+) channels control endothelin‐1‐induced mitogenesis and melanogenesis in primary human melanocytes. The Journal of Investigative Dermatology, 132(5), 1443–1451. https://doi.org/10.1038/jid.2011.478
Stratigos, A. J., Forsea, A. M., van der Leest, R. J., de Vries, E., Nagore, E., Bulliard, J. L., Trakatelli, M., Paoli, J., Peris, K., Hercogova, J., Bylaite, M., Maselis, T., Correia, O., & del Marmol, V. (2012). Euromelanoma: A dermatology‐led European campaign against nonmelanoma skin cancer and cutaneous melanoma. Past, present and future. The British Journal of Dermatology, 167(Suppl 2), 99–104. https://doi.org/10.1111/j.1365‐2133.2012.11092.x
Streisinger, G., Walker, C., Dower, N., Knauber, D., & Singer, F. (1981). Production of clones of homozygous diploid zebra fish (Brachydanio rerio). Nature, 291(5813), 293–296. https://doi.org/10.1038/291293a0
Sturm, R. A., Duffy, D. L., Box, N. F., Newton, R. A., Shepherd, A. G., Chen, W., Marks, L. H., Leonard, J. H., & Martin, N. G. (2003). Genetic association and cellular function of MC1R variant alleles in human pigmentation. Annals of the New York Academy of Sciences, 994, 348–358. https://doi.org/10.1111/j.1749‐6632.2003.tb03199.x
Sturm, R. A., Duffy, D. L., Zhao, Z. Z., Leite, F. P., Stark, M. S., Hayward, N. K., Martin, N. G., & Montgomery, G. W. (2008). A single SNP in an evolutionary conserved region within intron 86 of the HERC2 gene determines human blue‐brown eye color. American Journal of Human Genetics, 82(2), 424–431. https://doi.org/10.1016/j.ajhg.2007.11.005
Sulem, P., Gudbjartsson, D. F., Stacey, S. N., Helgason, A., Rafnar, T., Magnusson, K. P., Manolescu, A., Karason, A., Palsson, A., Thorleifsson, G., Jakobsdottir, M., Steinberg, S., Pálsson, S., Jonasson, F., Sigurgeirsson, B., Thorisdottir, K., Ragnarsson, R., Benediktsdottir, K. R., Aben, K. K., … Stefansson, K. (2007). Genetic determinants of hair, eye and skin pigmentation in Europeans. Nature Genetics, 39(12), 1443–1452. https://doi.org/10.1038/ng.2007.13
Szabó, G., Gerald, A. B., Pathak, M. A., & Fitzpatrick, T. B. (1969). Racial differences in the fate of melanosomes in human epidermis. Nature, 222(5198), 1081–1082. https://doi.org/10.1038/2221081a0
Takeuchi, S., Suzuki, H., Yabuuchi, M., & Takahashi, S. (1996). A possible involvement of melanocortin 1‐receptor in regulating feather color pigmentation in the chicken. Biochimica et Biophysica Acta, 1308(2), 164–168. https://doi.org/10.1016/0167‐4781(96)00100‐5
Taylor, S. C. (2002). Skin of color: Biology, structure, function, and implications for dermatologic disease. Journal of the American Academy of Dermatology, 46(2 Suppl), S41–S62. https://doi.org/10.1067/mjd.2002.120790
Theron, E., Hawkins, K., Bermingham, E., Ricklefs, R. E., & Mundy, N. I. (2001). The molecular basis of an avian plumage polymorphism in the wild: A melanocortin‐1‐receptor point mutation is perfectly associated with the melanic plumage morph of the bananaquit, Coereba Flaveola. Current Biology, 11(8), 550–557. https://doi.org/10.1016/s0960‐9822(01)00158‐0
Thody, A. J., Higgins, E. M., Wakamatsu, K., Ito, S., Burchill, S. A., & Marks, J. M. (1991). Pheomelanin as well as eumelanin is present in human epidermis. The Journal of Investigative Dermatology, 97(2), 340–344. https://doi.org/10.1111/1523‐1747.ep12480680
Thomas, D. B., McGraw, K. J., Butler, M. W., Carrano, M. T., Madden, O., & James, H. F. (2014). Ancient origins and multiple appearances of carotenoid‐pigmented feathers in birds. Proceedings of the Biological Sciences, 281(1788), 20140806. https://doi.org/10.1098/rspb.2014.0806
Thong, H. Y., Jee, S. H., Sun, C. C., & Boissy, R. E. (2003). The patterns of melanosome distribution in keratinocytes of human skin as one determining factor of skin colour. The British Journal of Dermatology, 149(3), 498–505. https://doi.org/10.1046/j.1365‐2133.2003.05473.x
Tishkoff, S. A., Reed, F. A., Friedlaender, F. R., Ehret, C., Ranciaro, A., Froment, A., Hirbo, J. B., Awomoyi, A. A., Bodo, J. M., Doumbo, O., Ibrahim, M., Juma, A. T., Kotze, M. J., Lema, G., Moore, J. H., Mortensen, H., Nyambo, T. B., Omar, S. A., Powell, K., … Williams, S. M. (2009). The genetic structure and history of Africans and African Americans. Science, 324(5930), 1035–1044. https://doi.org/10.1126/science.1172257
Tucci, S., & Akey, J. M. (2019). The long walk to African genomics. Genome Biology, 20(1), 130. https://doi.org/10.1186/s13059‐019‐1740‐1
Valverde, P., Healy, E., Jackson, I., Rees, J. L., & Thody, A. J. (1995). Variants of the melanocyte‐stimulating hormone receptor gene are associated with red hair and fair skin in humans. Nature Genetics, 11(3), 328–330. https://doi.org/10.1038/ng1195‐328
Villmoare, B., Kimbel, W. H., Seyoum, C., Campisano, C. J., DiMaggio, E. N., Rowan, J., Braun, D. R., Arrowsmith, J. R., & Reed, K. E. (2015). Paleoanthropology. Early homo at 2.8 Ma from Ledi‐Geraru, Afar, Ethiopia. Science, 347(6228), 1352–1355. https://doi.org/10.1126/science.aaa1343
Vogel, P., Read, R. W., Vance, R. B., Platt, K. A., Troughton, K., & Rice, D. S. (2008). Ocular albinism and hypopigmentation defects in Slc24a5−/− mice. Veterinary Pathology, 45(2), 264–279. https://doi.org/10.1354/vp.45‐2‐264
Wade, L. (2019). Light skin may be legacy of native American ancestors. Science, 363(6425), 333. https://doi.org/10.1126/science.363.6425.333
Wakamatsu, K., Kavanagh, R., Kadekaro, A. L., Terzieva, S., Sturm, R. A., Leachman, S., Abdel‐Malek, Z., & Ito, S. (2006). Diversity of pigmentation in cultured human melanocytes is due to differences in the type as well as quantity of melanin. Pigment Cell Research, 19(2), 154–162. https://doi.org/10.1111/j.1600‐0749.2006.00293.x
Wakamatsu, K., Ohtara, K., & Ito, S. (2009). Chemical analysis of late stages of pheomelanogenesis: Conversion of dihydrobenzothiazine to a benzothiazole structure. Pigment Cell & Melanoma Research, 22(4), 474–486. https://doi.org/10.1111/j.1755‐148X.2009.00580.x
Walker, A., El Demellawy, D., & Davila, J. (2017). Rickets: Historical, epidemiological, pathophysiological, and pathological perspectives. Academic Forensic Pathology, 7(2), 240–262. https://doi.org/10.23907/2017.024
Wang, F., Luo, Q., Chen, Y., Liu, Y., Xu, K., Adhikari, K., Cai, X., Liu, J., Li, Y., Liu, X., Ramirez‐Aristeguieta, L. M., Yuan, Z., Zhou, Y., Li, F. F., Jiang, B., Jin, L., Ruiz‐Linares, A., Yang, Z., Liu, F., & Wang, S. (2022). A genome‐wide scan on individual typology angle found variants at SLC24A2 associated with skin color variation in Chinese populations. The Journal of Investigative Dermatology, 142(4), 1223–1227.e1214. https://doi.org/10.1016/j.jid.2021.07.186
Wang, G., Liao, J., Tang, M., & Yu, S. (2018). Genetic variation in the MITF promoter affects skin colour and transcriptional activity in black‐boned chickens. British Poultry Science, 59(1), 21–27. https://doi.org/10.1080/00071668.2017.1379053
Wang, Y. H., Ho, T. L. F., Hariharan, A., Goh, H. C., Wong, Y. L., Verkaik, N. S., Lee, M. Y., Tam, W. L., van Gent, D. C., Venkitaraman, A. R., Sheetz, M. P., & Lane, D. P. (2022). Rapid recruitment of p53 to DNA damage sites directs DNA repair choice and integrity. Proceedings of the National Academy of Sciences of the United States of America, 119(10), e2113233119. https://doi.org/10.1073/pnas.2113233119
Watkins‐Chow, D. E., Incao, A. A., Rivas, C., Elliott, G., Garrett, L. J., & Pavan, W. J. (2023). The MFSD12 p.Tyr182His common variant is sufficient to alter mouse agouti coat color. Pigment Cell & Melanoma Research, 37, 259–264. https://doi.org/10.1111/pcmr.13144
Wei, A. H., Zang, D. J., Zhang, Z., Liu, X. Z., He, X., Yang, L., Wang, Y., Zhou, Z. Y., Zhang, M. R., Dai, L. L., Yang, X. M., & Li, W. (2013). Exome sequencing identifies SLC24A5 as a candidate gene for nonsyndromic oculocutaneous albinism. The Journal of Investigative Dermatology, 133(7), 1834–1840. https://doi.org/10.1038/jid.2013.49
Wilde, S., Timpson, A., Kirsanow, K., Kaiser, E., Kayser, M., Unterländer, M., Hollfelder, N., Potekhina, I. D., Schier, W., Thomas, M. G., & Burger, J. (2014). Direct evidence for positive selection of skin, hair, and eye pigmentation in Europeans during the last 5,000 y. Proceedings of the National Academy of Sciences of the United States of America, 111(13), 4832–4837. https://doi.org/10.1073/pnas.1316513111
Xi, Y., Liu, H., Li, L., Xu, Q., Liu, Y., Wang, L., Ma, S., Wang, J., Bai, L., Zhang, R., & Han, C. (2020). Transcriptome reveals multi pigmentation genes affecting Dorsoventral pattern in avian body. Frontiers in Cell and Development Biology, 8, 560766. https://doi.org/10.3389/fcell.2020.560766
Xiang, K., Ouzhuluobu, P., Yang, Z., Zhang, X., Cui, C., & Su, B. (2013). Identification of a Tibetan‐specific mutation in the hypoxic gene EGLN1 and its contribution to high‐altitude adaptation. Molecular Biology and Evolution, 30(8), 1889–1898. https://doi.org/10.1093/molbev/mst090
Yang, Z., Bai, C., Pu, Y., Kong, Q., Guo, Y., Ouzhuluobu, Gengdeng, Liu, X., Zhao, Q., Qiu, Z., Zheng, W., He, Y., Lin, Y., Deng, L., Zhang, C., Xu, S., Peng, Y., Xiang, K., Zhang, X., … Su, B. (2022). Genetic adaptation of skin pigmentation in highland Tibetans. Proceedings of the National Academy of Sciences of the United States of America, 119(40), e2200421119. https://doi.org/10.1073/pnas.2200421119
Yang, Z., Shi, H., Ma, P., Zhao, S., Kong, Q., Bian, T., Gong, C., Zhao, Q., Liu, Y., Qi, X., Zhang, X., Han, Y., Liu, J., Li, Q., Chen, H., & Su, B. (2018). Darwinian positive selection on the pleiotropic effects of KITLG explain skin pigmentation and winter temperature adaptation in Eurasians. Molecular Biology and Evolution, 35(9), 2272–2283. https://doi.org/10.1093/molbev/msy136
Yang, Z., Zhong, H., Chen, J., Zhang, X., Zhang, H., Luo, X., & Su, B. (2016). A genetic mechanism for convergent skin lightening during recent human evolution. Molecular Biology and Evolution, 33(5), 1177–1187. https://doi.org/10.1093/molbev/msw003
Yardman‐Frank, J. M., & Fisher, D. E. (2021). Skin pigmentation and its control: From ultraviolet radiation to stem cells. Experimental Dermatology, 30(4), 560–571. https://doi.org/10.1111/exd.14260
Yi, X., Liang, Y., Huerta‐Sanchez, E., Jin, X., Cuo, Z. X., Pool, J. E., Xu, X., Jiang, H., Vinckenbosch, N., Korneliussen, T. S., Zheng, H., Liu, T., He, W., Li, K., Luo, R., Nie, X., Wu, H., Zhao, M., Cao, H., … Wang, J. (2010). Sequencing of 50 human exomes reveals adaptation to high altitude. Science, 329(5987), 75–78. https://doi.org/10.1126/science.1190371
Yuasa, I., Umetsu, K., Watanabe, G., Nakamura, H., Endoh, M., & Irizawa, Y. (2004). MATP polymorphisms in Germans and Japanese: The L374F mutation as a population marker for Caucasoids. International Journal of Legal Medicine, 118(6), 364–366. https://doi.org/10.1007/s00414‐004‐0490‐z
Zaorska, K., Zawierucha, P., & Nowicki, M. (2019). Prediction of skin color, tanning and freckling from DNA in polish population: Linear regression, random forest and neural network approaches. Human Genetics, 138(6), 635–647. https://doi.org/10.1007/s00439‐019‐02012‐w
Zhang, X., Qi, Y., Pang, Y., Yuan, B., & Li, X. (2023). Identification of polymorphisms in the HERC2‐OCA2 gene locus and their association with feather color in quail. The Journal of Poultry Science, 60(2), 2023013. https://doi.org/10.2141/jpsa.2023013
Zhou, S., Zeng, H., Huang, J., Lei, L., Tong, X., Li, S., Zhou, Y., Guo, H., Khan, M., Luo, L., Xiao, R., Chen, J., & Zeng, Q. (2021). Epigenetic regulation of melanogenesis. Ageing Research Reviews, 69, 101349. https://doi.org/10.1016/j.arr.2021.101349
Zhu, W., Wang, L., Dong, Z., Chen, X., Song, F., Liu, N., Yang, H., & Fu, J. (2016). Comparative transcriptome analysis identifies candidate genes related to skin color differentiation in red tilapia. Scientific Reports, 6, 31347. https://doi.org/10.1038/srep31347

Auteurs

Jiuming Liu (J)

Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University, Zhengzhou, China.

Habtom K Bitsue (HK)

Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University, Zhengzhou, China.

Zhaohui Yang (Z)

Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University, Zhengzhou, China.

Classifications MeSH