Born blonde: a recessive loss-of-function mutation in the melanocortin 1 receptor is associated with cream coat coloration in Antarctic fur seals

Peters L, Humble E, Kröcker N, Fuchs B, Forcada J, Hoffman J (2016)
Ecology and Evolution 6(16): 5705-5717.

Zeitschriftenaufsatz | Veröffentlicht| Englisch
 
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Peters, Lucy; Humble, EmilyUniBi ; Kröcker, Nicole; Fuchs, Birgit; Forcada, Jaume; Hoffman, JosephUniBi
Abstract / Bemerkung
Although the genetic basis of color variation has been extensively studied in humans and domestic animals, the genetic polymorphisms responsible for different color morphs remain to be elucidated in many wild vertebrate species. For example, hypopigmentation has been observed in numerous marine mammal species but the underlying mutations have not been identified. A particularly compelling candidate gene for explaining color polymorphism is the melanocortin 1 receptor (MC1R), which plays a key role in the regulation of pigment production. We therefore used Antarctic fur seals (Arctocephalus gazella) as a highly tractable marine mammal system with which to test for an association between nucleotide variation at the MC1R and melanin-based coat color phenotypes. By sequencing 70 wild-type individuals with dark-colored coats and 26 hypopigmented individuals with cream-colored coats, we identified a nonsynonymous mutation that results in the substitution of serine with phenylalanine at an evolutionarily highly conserved structural domain. All of the hypopigmented individuals were homozygous for the allele coding for phenylalanine, consistent with a recessive loss-of-function allele. In order to test for cryptic population structure, which can generate artefactual associations, and to evaluate whether homozygosity at the MC1R could be indicative of low genome-wide heterozygosity, we also genotyped all of the individuals at 50 polymorphic microsatellite loci. We were unable to detect any population structure and also found that wild-type and hypopigmented individuals did not differ significantly in their standardized multilocus heterozygosity. Such a lack of association implies that hypopigmented individuals are unlikely to suffer disproportionately from inbreeding depression, and hence, we have no reason to believe that they are at a selective disadvantage in the wider population.
Erscheinungsjahr
2016
Zeitschriftentitel
Ecology and Evolution
Band
6
Ausgabe
16
Seite(n)
5705-5717
ISSN
2045-7758
Finanzierungs-Informationen
Article Processing Charge funded by the Deutsche Forschungsgemeinschaft and the Open Access Publication Fund of Bielefeld University.
Page URI
https://pub.uni-bielefeld.de/record/2904987

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Peters L, Humble E, Kröcker N, Fuchs B, Forcada J, Hoffman J. Born blonde: a recessive loss-of-function mutation in the melanocortin 1 receptor is associated with cream coat coloration in Antarctic fur seals. Ecology and Evolution. 2016;6(16):5705-5717.
Peters, L., Humble, E., Kröcker, N., Fuchs, B., Forcada, J., & Hoffman, J. (2016). Born blonde: a recessive loss-of-function mutation in the melanocortin 1 receptor is associated with cream coat coloration in Antarctic fur seals. Ecology and Evolution, 6(16), 5705-5717. doi:10.1002/ece3.2290
Peters, L., Humble, E., Kröcker, N., Fuchs, B., Forcada, J., and Hoffman, J. (2016). Born blonde: a recessive loss-of-function mutation in the melanocortin 1 receptor is associated with cream coat coloration in Antarctic fur seals. Ecology and Evolution 6, 5705-5717.
Peters, L., et al., 2016. Born blonde: a recessive loss-of-function mutation in the melanocortin 1 receptor is associated with cream coat coloration in Antarctic fur seals. Ecology and Evolution, 6(16), p 5705-5717.
L. Peters, et al., “Born blonde: a recessive loss-of-function mutation in the melanocortin 1 receptor is associated with cream coat coloration in Antarctic fur seals”, Ecology and Evolution, vol. 6, 2016, pp. 5705-5717.
Peters, L., Humble, E., Kröcker, N., Fuchs, B., Forcada, J., Hoffman, J.: Born blonde: a recessive loss-of-function mutation in the melanocortin 1 receptor is associated with cream coat coloration in Antarctic fur seals. Ecology and Evolution. 6, 5705-5717 (2016).
Peters, Lucy, Humble, Emily, Kröcker, Nicole, Fuchs, Birgit, Forcada, Jaume, and Hoffman, Joseph. “Born blonde: a recessive loss-of-function mutation in the melanocortin 1 receptor is associated with cream coat coloration in Antarctic fur seals”. Ecology and Evolution 6.16 (2016): 5705-5717.
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4 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Age- and quality-dependent DNA methylation correlate with melanin-based coloration in a wild bird.
Soulsbury CD, Lipponen A, Wood K, Mein CA, Hoffman JI, Lebigre C., Ecol Evol 8(13), 2018
PMID: 30038756
RAD Sequencing and a Hybrid Antarctic Fur Seal Genome Assembly Reveal Rapidly Decaying Linkage Disequilibrium, Global Population Structure and Evidence for Inbreeding.
Humble E, Dasmahapatra KK, Martinez-Barrio A, Gregório I, Forcada J, Polikeit AC, Goldsworthy SD, Goebel ME, Kalinowski J, Wolf JBW, Hoffman JI., G3 (Bethesda) 8(8), 2018
PMID: 29954843
A global cline in a colour polymorphism suggests a limited contribution of gene flow towards the recovery of a heavily exploited marine mammal.
Hoffman JI, Bauer E, Paijmans AJ, Humble E, Beckmann LM, Kubetschek C, Christaller F, Kröcker N, Fuchs B, Moreras A, Shihlomule YD, Bester MN, Cleary AC, De Bruyn PJN, Forcada J, Goebel ME, Goldsworthy SD, Guinet C, Hoelzel AR, Lydersen C, Kovacs KM, Lowther A., R Soc Open Sci 5(10), 2018
PMID: 30473858

96 References

Daten bereitgestellt von Europe PubMed Central.

Leucistic South American sea lion in Chile, with a review of anomalously color in otariids
AUTHOR UNKNOWN, 2008
Rare piebald and partially leucistic Antarctic fur seals, Arctocephalus gazella, at Cape Shirreff, Livingston Island, Antarctica
AUTHOR UNKNOWN, 2009
The Present Status of the Antarctic fur seal Arctocephalus gazella at South Shetland Islands
AUTHOR UNKNOWN, 1978
Long‐term preservation of whale skin for DNA analysis
AUTHOR UNKNOWN, 1991

AUTHOR UNKNOWN, 1994
Fingerprinting G-protein-coupled receptors.
Attwood TK, Findlay JB., Protein Eng. 7(2), 1994
PMID: 8170923
The PRINTS database: a fine‐grained protein sequence annotation and analysis resource‐its status in 2012
AUTHOR UNKNOWN, 2012
Winter population of pinnipeds about Guadaloupe, San Benito, and Cedros Islands, Baja California
AUTHOR UNKNOWN, 1952
Pleiotropic effects of pigmentation genes in horses.
Bellone RR., Anim. Genet. 41 Suppl 2(), 2010
PMID: 21070283
Leucistic southern elephant seal at Marion Island?
AUTHOR UNKNOWN, 2008
The fur seal of South Georgia
AUTHOR UNKNOWN, 1968
An abberantly pigmented southern elephant seal (Mirounga leonina) at Isles Kerguelen, South Indian Ocean
AUTHOR UNKNOWN, 2000
Accurate prediction of the functional significance of single nucleotide polymorphisms and mutations in the ABCA1 gene
AUTHOR UNKNOWN, 2005
Leucistic antarctic fur seal Arctocephalus gazella at marion island
AUTHOR UNKNOWN, 2007
Microsatellites from the Atlantic walrus Odobenus rosmarus rosmarus.
Buchanan FC, Maiers LD, Thue TD, De March BG, Stewart RE., Mol. Ecol. 7(8), 1998
PMID: 9711867
Fitness in common buzzards at the cross‐point of opposite melanin‐parasite interactions
AUTHOR UNKNOWN, 2008
Slc7a11 gene controls production of pheomelanin pigment and proliferation of cultured cells.
Chintala S, Li W, Lamoreux ML, Ito S, Wakamatsu K, Sviderskaya EV, Bennett DC, Park YM, Gahl WA, Huizing M, Spritz RA, Ben S, Novak EK, Tan J, Swank RT., Proc. Natl. Acad. Sci. U.S.A. 102(31), 2005
PMID: 16037214
Parasite-mediated selection against inbred Soay sheep in a free-living, island population.
Coltman DW, Pilkington JG, Smith JA, Pemberton JM., Evolution 53(4), 1999
PMID: IND22030991
ProtTest 3: fast selection of best-fit models of protein evolution.
Darriba D, Taboada GL, Doallo R, Posada D., Bioinformatics 27(8), 2011
PMID: 21335321
Dinucleotide microsatellite markers from the Antarctic seals and their use in other pinnipeds
AUTHOR UNKNOWN, 2002
Melanocortin 1 receptor variants: functional role and pigmentary associations.
Dessinioti C, Antoniou C, Katsambas A, Stratigos AJ., Photochem. Photobiol. 87(5), 2011
PMID: 21749400
Bayesian phylogenetics with BEAUti and the BEAST 1.7.
Drummond AJ, Suchard MA, Xie D, Rambaut A., Mol. Biol. Evol. 29(8), 2012
PMID: 22367748
Molecular genetics and evolution of melanism in the cat family.
Eizirik E, Yuhki N, Johnson WE, Menotti-Raymond M, Hannah SS, O'Brien SJ., Curr. Biol. 13(5), 2003
PMID: 12620197

AUTHOR UNKNOWN, 2008
First record of an albino bottlenose dolphin (Tursiops truncatus) in the Gulf of Mexico, with a review of anomalously white cetaceans
AUTHOR UNKNOWN, 1999
An update on anomalously white cetaceans, including the first account for the pantropical spotted dolphin (Stenella attenuata Graffmani)
AUTHOR UNKNOWN, 2004
The melanocortin system.
Gantz I, Fong TM., Am. J. Physiol. Endocrinol. Metab. 284(3), 2003
PMID: 12556347
Interspecific microsatellite markers for the study of pinniped populations.
Gemmell NJ, Allen PJ, Goodman SJ, Reed JZ., Mol. Ecol. 6(7), 1997
PMID: 9226947

AUTHOR UNKNOWN, 1982
Pheomelanin coat colour dilution in French cattle breeds is not correlated with the TYR, TYRP1 and DCT transcription levels.
Guibert S, Girardot M, Leveziel H, Julien R, Oulmouden A., Pigment Cell Res. 17(4), 2004
PMID: 15250935
BioEdit: a user‐friendly biological sequence alignment editor and analysis program for windows 95/98/NT
AUTHOR UNKNOWN, 1999
New polymorphic microsatellite markers for California sea lions (Zalophus californianus)
AUTHOR UNKNOWN, 2005
A single amino acid mutation contributes to adaptive beach mouse color pattern.
Hoekstra HE, Hirschmann RJ, Bundey RA, Insel PA, Crossland JP., Science 313(5783), 2006
PMID: 16825572
Alpha‐male paternity in elephant seals
AUTHOR UNKNOWN, 1999
A novel approach for mining polymorphic microsatellite markers in silico.
Hoffman JI, Nichols HJ., PLoS ONE 6(8), 2011
PMID: 21853104
Bayesian inference of a historical bottleneck in a heavily exploited marine mammal.
Hoffman JI, Grant SM, Forcada J, Phillips CD., Mol. Ecol. 20(19), 2011
PMID: 21895820
Characterization of eight microsatellite loci in Steller sea lions (Eumetopias jubatus)
HUEBINGER RM, LOUIS EEJ, GELATT T, REA LD, BICKHAM JW., Mol. Ecol. Notes 7(6), 2007
PMID: IND43974463
A draft fur seal genome provides insights into factors affecting SNP validation and how to mitigate them.
Humble E, Martinez-Barrio A, Forcada J, Trathan PN, Thorne MA, Hoffmann M, Wolf JB, Hoffman JI., Mol Ecol Resour 16(4), 2016
PMID: 26683564
Red coat color in Holstein cattle is associated with a deletion in the MSHR gene.
Joerg H, Fries HR, Meijerink E, Stranzinger GF., Mamm. Genome 7(4), 1996
PMID: 8661706
Genetics of pigmentation in dogs and cats.
Kaelin CB, Barsh GS., Annu Rev Anim Biosci 1(), 2013
PMID: 25387014
Exclusion of melanocortin-1 receptor (mc1r) and agouti as candidates for dominant black in dogs.
Kerns JA, Olivier M, Lust G, Barsh GS., J. Hered. 94(1), 2003
PMID: 12692166
Melanocortin receptor 1 (MC1R) mutations and coat color in pigs.
Kijas JM, Wales R, Tornsten A, Chardon P, Moller M, Andersson L., Genetics 150(3), 1998
PMID: 9799269
The role of melanocyte-stimulating hormone (MSH) receptor in bovine coat color determination.
Klungland H, Vage DI, Gomez-Raya L, Adalsteinsson S, Lien S., Mamm. Genome 6(9), 1995
PMID: 8535072
Maladaptive mate choice maintained by heterozygote advantage.
Kruger O, Lindstrom J, Amos W., Evolution 55(6), 2001
PMID: 11475056
A supergene determines highly divergent male reproductive morphs in the ruff.
Kupper C, Stocks M, Risse JE, Dos Remedios N, Farrell LL, McRae SB, Morgan TC, Karlionova N, Pinchuk P, Verkuil YI, Kitaysky AS, Wingfield JC, Piersma T, Zeng K, Slate J, Blaxter M, Lank DB, Burke T., Nat. Genet. 48(1), 2015
PMID: 26569125
Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax).
Lamichhaney S, Fan G, Widemo F, Gunnarsson U, Thalmann DS, Hoeppner MP, Kerje S, Gustafson U, Shi C, Zhang H, Chen W, Liang X, Huang L, Wang J, Liang E, Wu Q, Lee SM, Xu X, Hoglund J, Liu X, Andersson L., Nat. Genet. 48(1), 2015
PMID: 26569123
Mammalian melanism: natural selection in black and white.
Majerus ME, Mundy NI., Trends Genet. 19(11), 2003
PMID: 14585605
The capture and handling of female South‐American fur seals and their pups
AUTHOR UNKNOWN, 1992
A mutation in the MATP gene causes the cream coat colour in the horse.
Mariat D, Taourit S, Guerin G., Genet. Sel. Evol. 35(1), 2003
PMID: 12605854
PANTHER version 10: expanded protein families and functions, and analysis tools.
Mi H, Poudel S, Muruganujan A, Casagrande JT, Thomas PD., Nucleic Acids Res. 44(D1), 2015
PMID: 26578592
The role of the agouti gene in the yellow obese syndrome
AUTHOR UNKNOWN, 1997
The InterPro protein families database: the classification resource after 15 years.
Mitchell A, Chang HY, Daugherty L, Fraser M, Hunter S, Lopez R, McAnulla C, McMenamin C, Nuka G, Pesseat S, Sangrador-Vegas A, Scheremetjew M, Rato C, Yong SY, Bateman A, Punta M, Attwood TK, Sigrist CJ, Redaschi N, Rivoire C, Xenarios I, Kahn D, Guyot D, Bork P, Letunic I, Gough J, Oates M, Haft D, Huang H, Natale DA, Wu CH, Orengo C, Sillitoe I, Mi H, Thomas PD, Finn RD., Nucleic Acids Res. 43(Database issue), 2014
PMID: 25428371
The genetic basis of adaptive melanism in pocket mice.
Nachman MW, Hoekstra HE, D'Agostino SL., Proc. Natl. Acad. Sci. U.S.A. 100(9), 2003
PMID: 12704245
Melanocortin 1 receptor variation in the domestic dog.
Newton JM, Wilkie AL, He L, Jordan SA, Metallinos DL, Holmes NG, Jackson IJ, Barsh GS., Mamm. Genome 11(1), 2000
PMID: 10602988
The genome sequencing of an albino Western lowland gorilla reveals inbreeding in the wild
AUTHOR UNKNOWN, 2013
Inference of population structure using multilocus genotype data.
Pritchard JK, Stephens M, Donnelly P., Genetics 155(2), 2000
PMID: 10835412
BEDTools: a flexible suite of utilities for comparing genomic features.
Quinlan AR, Hall IM., Bioinformatics 26(6), 2010
PMID: 20110278
Genepop (version 1.2) – population genetics software for exact tests of ecumenicism
AUTHOR UNKNOWN, 1995
Inheritance and population structure of the white-phased "Kermode" black bear.
Ritland K, Newton C, Marshall HD., Curr. Biol. 11(18), 2001
PMID: 11566108
Pigmentation phenotypes of variant extension locus alleles result from point mutations that alter MSH receptor function.
Robbins LS, Nadeau JH, Johnson KR, Kelly MA, Roselli-Rehfuss L, Baack E, Mountjoy KG, Cone RD., Cell 72(6), 1993
PMID: 8458079
Nuclear gene indicates coat-color polymorphism in mammoths.
Rompler H, Rohland N, Lalueza-Fox C, Willerslev E, Kuznetsova T, Rabeder G, Bertranpetit J, Schoneberg T, Hofreiter M., Science 313(5783), 2006
PMID: 16825562
The structure and function of G-protein-coupled receptors.
Rosenbaum DM, Rasmussen SG, Kobilka BK., Nature 459(7245), 2009
PMID: 19458711

AUTHOR UNKNOWN, 1989
Isolation and cross‐species amplification of novel microsatellite loci in a charismatic marine mammal species, the northern elephant seal (Mirounga angustirostris)
AUTHOR UNKNOWN, 2013
Loss of function mutations of the human melanocortin 1 receptor are common and are associated with red hair.
Schioth HB, Phillips SR, Rudzish R, Birch-Machin MA, Wikberg JE, Rees JL., Biochem. Biophys. Res. Commun. 260(2), 1999
PMID: 10403794
The genetics of cream coat color in dogs.
Schmutz SM, Berryere TG., J. Hered. 98(5), 2007
PMID: 17485734
TYRP1 and MC1R genotypes and their effects on coat color in dogs.
Schmutz SM, Berryere TG, Goldfinch AD., Mamm. Genome 13(7), 2002
PMID: 12140685
Chemical fingerprints encode mother-offspring similarity, colony membership, relatedness, and genetic quality in fur seals.
Stoffel MA, Caspers BA, Forcada J, Giannakara A, Baier M, Eberhart-Phillips L, Muller C, Hoffman JI., Proc. Natl. Acad. Sci. U.S.A. 112(36), 2015
PMID: 26261311
inbreedR: An R package for the analysis of inbreeding based on genetic markers
AUTHOR UNKNOWN, 2016
A possible involvement of melanocortin 1-receptor in regulating feather color pigmentation in the chicken.
Takeuchi S, Suzuki H, Yabuuchi M, Takahashi S., Biochim. Biophys. Acta 1308(2), 1996
PMID: 8764834
PANTHER: a library of protein families and subfamilies indexed by function.
Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, Daverman R, Diemer K, Muruganujan A, Narechania A., Genome Res. 13(9), 2003
PMID: 12952881
Applications for protein sequence-function evolution data: mRNA/protein expression analysis and coding SNP scoring tools.
Thomas PD, Kejariwal A, Guo N, Mi H, Campbell MJ, Muruganujan A, Lazareva-Ulitsky B., Nucleic Acids Res. 34(Web Server issue), 2006
PMID: 16912992
Primer3Plus, an enhanced web interface to Primer3.
Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA., Nucleic Acids Res. 35(Web Server issue), 2007
PMID: 17485472
First confirmed record of a leucistic Antarctic fur seal pup born outside the Scotia Arc Islands
AUTHOR UNKNOWN, 2015
Development of new microsatellite loci and evaluation of loci from other pinniped species for the Galapagos sea lion (Zalophus californianus wollebaeki)
AUTHOR UNKNOWN, 2005
Effects of population structure on genetic association studies.
Xu H, Shete S., BMC Genet. 6 Suppl 1(), 2005
PMID: 16451565
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