Abstract
Feather colours are used by avian species for defense, adaptation and signaling. Melanocortin-1 receptor (MC1R) gene is one of the genes responsible for feather colour. This study identified selection signatures in MC1R gene of Nigerian indigenous turkeys (NIT) using British United turkeys (BUT) as control breed to investigate the evolutionary processes that have shaped NIT with various feather colours. Complete MC1R gene of 146 NIT (76 males and 70 females) and 32 BUT (18 males and 14 females) were sequenced. Transition/transversion and codon usage biases were predicted using MEGA v6 software. The selective force acting on the gene was predicted using HyPhy software. The FST values were estimated using Arlequin v3.5. The highest transition/transversion bias was predicted for white BUT (1.00) while the lowest was predicted for black NIT (0.50). Negative dN-dS values, indicative of purifying selection, were observed in MC1R gene of all the turkeys. The highest pairwise FST was observed between the MC1R gene of white BUT and black NIT while the least was observed between lavender NIT and white NIT. No recombination event was observed in black NIT and white BUT. The relative synonymous codon usage was the same among different colours for some codons. Presence of purifying selection in MC1R gene of all the turkeys with different feather colours confirms that the gene plays role in many biological processes such as feather colouration, behaviour, pain perception, immunity, growth and adaptation. The results also suggested that the genetic mechanisms generating different feather colours in turkeys are conserved.
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The data has been deposited to GenBank with accession number MF360992.1.
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References
Adams, P.E., Crist, A.B., Young, E.M., Willis, J.H., Phillips, P.C., & Fierst, J.L. (2021). Slow recovery from inbreeding depression generated by the complex genetic architecture of segregating deleterious mutations. Molecular Biology and Evolution, https://doi.org/10.1093/molbev/msab330.
Bergstrom, C.T., & Pritchard, J. (1998). Germline bottlenecks and the evolutionary maintenance of mitochondrial genome. Genetics, 149(4), 2135-2146.
Biswas, R., Panja, A.S., & Bandopadhyay, R. (2019). In silico analyses of burial codon bias among species of Dipterocarpaceae through molecular and phylogenetic data. Evolutionary Bioinformatics, 15, 1-12. https://doi.org/10.1177/1176934319834888.
Bonhomme, M., Chevalet, C., Servin, B., Boitard, S., Abdallah, J., Blott, S., & SanCristobal, M. (2010). Detecting selection in population trees: The Lewontin and Krakauer Test extended. Genetics, 186,241–262. https://doi.org/10.1534/genetics.104.117275.
Brunet, T.D.P., Doolittle, W.F., & Bielawski, J.P. (2021). The role of purifying selection in the origin and maintenance of complex function. Studies in History and Philosophy of Science, 87, 125-135. https://doi.org/10.1016/j.shpsa.2021.03.005.
Burtt, E. (1986). An analysis of physical, physiological and optical aspects of avian coloration with emphasis on wood-warblers. Ornithological Monographs, 38, 1–126.
Cavassim, M.I.A., Andersen, S.U., Bataillou, T., & Schierup, M.H. (2021). Recombination facilitates adaptive evolution in Rhizobial soil bacteria. Molecular Biology and Evolution, 38(12), 5480-5490. https://doi.org/10.1093/molbev/msab247.
Charlesworth, D. (2006). Balancing selection and its effects on sequences in nearby genome regions. PLoS Genetics, 2, e64. https://doi.org/10.1371/journal.pgen.0020064.
Charlesworth, D., & Willis, J.H. (2009). The genetics of inbreeding depression. Nature Reviews Genetics, 10, 783– 796. https://doi.org/10.1038/nrg2664.
Delhey, K. (2015). The colour of an avifauna: A quantitative analysis of the colour of Australian birds. Scientific Reports, 5, 1–12. https://doi.org/10.1038/srep18514.
Demontis, D., Pertoldi, C., Loeschcke, V., Mikkelsen, K., Axelsson, T., & Kristensen, T.N. (2009). Efficiency of selection, as measured by single nucleotide polymorphism variation, is dependent on inbreeding rate in Drosophila melanogaster. Molecular Ecology, 18, 4551– 4563. https://doi.org/10.1111/j.1365-294X.2009.04366.x.
Duchêne, S., Ho, S.Y., & Holmes, E.C. (2015). Declining transition/transversion ratios through time reveal limitations to the accuracy of nucleotide substitution models. BMC Evolutionary Biology, 15, 36. https://doi.org/10.1186/s12862-015-0312-6.
Durosaro, S.O., Ilori, B.M., Ajani, A.O., & Ozoje, M.O. (2019). Description of body conformation of Nigerian indigenous turkeys using exploratory factor analysis. Nigerian Journal of Animal Science, 21(2), 30-38.
Excoffier, L., & Lischer, H.E.L. (2010). Arlequin Suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567. https://doi.org/10.1111/j.1755-0998.2010.02847.x.
Fowler, K., & Whitlock, M.C. (1999). The distribution of phenotypic variance with inbreeding. Evolution, 53, 1143–1156. https://doi.org/10.2307/2640818.
Fox, C.W. (2012). The effect of inbreeding on natural selection in a seed-feeding beetle. Journal of Evolutionary Biology, 26, 88-93. https://doi.org/10.1111/jeb.12027.
Fu, Y.X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915–925.
Goldstein, G., Flory, K., Browne, B., Majid, S., Ichida, J.M., & Burtt, E.H. (2004). Bacterial degradation of black and white feathers. The American Ornithologists’ Union, 121, 656–659.
Hall, T.A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
Hershberg, R., & Petrov, D.A. (2008). Selection on codon bias. Annual Review of Genetics, 42, 287–99. https://doi.org/10.1146/annurev.genet.42.110807.091442.
Hudson, R.R., & Kaplan, N.L. (1985). Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics, 111, 147-164.
Ikemura, T. (1985). Codon usage and tRNA content in unicellular and multicellular organisms. Molecular Biology and Evolution, 2(1), 13–34. https://doi.org/10.1093/oxfordjournals.molbev.a040335.
Ilori, B.M., Durosaro, S.O., Isidahomen, C.E., Uthman, N.A., Komolafe, D.T., Akano, K., & Ozoje, M.O. (2019). Effect of Feather Color on Heat Tolerance Traits and Growth Performance of Nigerian Indigenous Turkey. The Pacific Journal of Science and Technology, 20 (2), 231-240.
Ivimey-Cook, E., Bricout, S., Candela, V., Maklakov, A.A., & Berg, E.C. (2021). Inbreeding reduces fitness of seed beetles under thermal stress. Journal of Evolutionary Biology, 34(9), 1386-1396. https://doi.org/10.1111/jeb.13899.
Keller, S.R., & Taylor, D.R. (2008). History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection. Ecology Letters, 11, 852-866. https://doi.org/10.1111/j.1461-0248.2008.01188.x.
Keller, I., Bensasson, D., & Nichols, R.A. (2007). Transition-transversion bias is not universal: A counter example from grasshopper pseudo genes. PLOS Genetics, 3(2):e22. https://doi.org/10.1371/journal.pgen.0030022.
Kerje, S., Sharma, P., Gunnarsson, U., Kim, H., Bagchi, S., Fredriksson, R., & Andersson, L. (2004). The Dominant white, Dun and Smoky color variants in chicken are associated with insertion/deletion polymorphisms in the PMEL17 gene. Genetics, 168, 1507–1518. https://doi.org/10.1534/genetics.104.027995.
Kimchi-Sarfaty, C., Oh, J.M., Kim, I.W., Sauna, Z.E., Calcagno, A.M., Ambudkar, S.V., & Gottesman, M.M. (2007). A ‘silent’ polymorphism in the MDR1 gene changes substrate specificity. Science, 315(5811), 525–528. https://doi.org/10.1126/science.1135308.
Knight, R.D., Freeland, S.J., & Landweber, L.F. (2001). A simple model based on mutation and selection explains trends in codon and amino-acid usage and GC composition within and across genomes. Genome Biology, 2, RESEARCH0010. https://doi.org/10.1186/gb-2001-2-4-research0010.
Kreitman, M. (2000). Methods to detect selection in populations with applications to the human. Annual Review of Genomics and Human Genetics, 1, 539–559. https://doi.org/10.1146/annurev.genom.1.1.539.
Li, W.H., Luo, C.C., & Wu, C.I. (1985). Evolution of DNA sequences. In: R.J. MacIntyre (Eds.), Molecular Evolutionary Genetics (pp. 20-27). New York: Plenum.
Li, N., Sun, M., Jiang, Z., Shu, H., & Zhang, S. (2016). Genome-wide analysis of the synonymous codon usage patterns in apple. Journal of integrative agriculture, 15(5), 983-991. https://doi.org/10.1016/S2095-3119(16)61333-3.
Lillie, M., Honaker, C.F., Siegel, P.B., & Carlborg, O. (2019). Bidirectional selection for body weight on standing genetic variation in a chicken model. Genes/Genomes/Genetics, 9, 1165-1173. https://doi.org/10.1534/g3.119.400038.
Liu, H., & Zhang, J. (2019). Yeast spontaneous mutation rate and spectrum vary with environment. Current Biology, 29(10), 1584-1591. https://doi.org/10.1016/j.cub.2019.03.054.
Lynch, M. (2010). Rate, molecular spectrum, and consequences of human mutation. Proceedings of the National Academy of Science of United States of America, 1073, 961–968. https://doi.org/10.1073/pnas.0912629107.
Lyons, D.M., & Lauring, A.S. (2017). Evidence for the selective bias of transition-to-transversion substitution bias in two RNA viruses. Molecular Biology and Evolution, 34(12), 3205-3215. https://doi.org/10.1093/molbev/msx251.
McGraw, K.J., Safra, R.J., Evans, M.R., & Wakamatsu, K. (2004). European barn swallows use melanin pigments to color their feathers brown. Behavioural Ecology, 15, 889–891. https://doi.org/10.1093/beheco/arh109.
Mundy, N.I. (2005). A window on the genetics of evolution: MC1R and feather colouration in birds. Proceedings Biology Sciences, 272(1573), 1633–1640. https://doi.org/10.1098/rspb.2005.3107.
Mundy, N.I., & Kelly, J. (2003). Evolution of a pigmentation gene, the Melanocortin-1 receptor, in primates. American Journal of Physical Anthropology, 121, 67-80. https://doi.org/10.1002/ajpa.10169.
Myers, S.R., & Griffiths, R.C. (2003). Bounds on the minimum number of recombination events in a sample history. Genetics, 163(1), 375-394.
Negro, J.J., Blasco, R., Rosell, J., & Finlayson, C. (2016). Finlayson C. Potential exploitation of avian resources by fossil hominins: An overview from ethnographic and historical data. Quaternary International, 421, 6-11. https://doi.org/10.1016/j.quaint.2015.09.034.
Nielsen, R. (2005). Molecular signatures of natural selection. Annual Review of Genetics, 39, 197–218. https://doi.org/10.1146/annurev.genet.39.073003.112420.
Rosenberg, M.S., Subramanian, S., & Kumar, S. (2003). Patterns of transitional mutation biases within and among mammalian genomes. Molecular Biology and Evolution, 20, 988–993. https://doi.org/10.1093/molbev/msg113.
Roth, A., Anisimova, M., & Cannarozzi, G.N. (2015). Measuring usage bias codon usage bias. In G.M. Cannarozzi & A. Schneider (Eds.), Codon evolution: Mechanisms and models (pp. 189-217). United Kingdom, Oxford.
Rozaz, J., Ferrer-Mata, A., Sanchez-DelBarrio, J.C., Guirao-Rico, S., Librado, P, Ramos-Onsins, S.E., & Sanchez-Gracia, A. (2017). DnaSP v6: DNA sequence polymorphism analysis of large dataset. Molecular Biology and Evolution, 34, 3299-3302. https://doi.org/10.1093/molbev/msx248.
Sanjukta, R., Farooqi, M.S., Sharma, N., Rai, A., Mishra, D.C., & Singh, D.P. (2012). Trends in the codon usage patterns of Chromohalobacter salexigens genes. Bioinformation, 8, 1087–1095. https://doi.org/10.6026/97320630081087.
Schlötterer, C. (2003). Hitchhiking mapping – functional genomics from the population genetics perspective. Trends in Genetics, 19, 32–38. https://doi.org/10.1016/s0168-9525(02)00012-4.
de Simoni Gouveia, J.J., da Silva, M.V., Paiva, S.R., & de Oliveira, S.M. (2014). Identification of selection signatures in livestock species. Genetics and Molecular Biology, 37(2), 330–342. https://doi.org/10.1590/s1415-47572014000300004.
Stephan, W. (2010). Genetic hitchhiking vs background selection: The controversy and its implication. Philosophical Transactions of the Royal Society: Biological Sciences, 365, 1245-1253. https://doi.org/10.1098/rstb.2009.0278.
Stoltzfus, A., & Norris, R.W. (2016). On the Causes of Evolutionary Transition:Transversion Bias. Molecular Biology and Evolution, 33(3), 595–602. https://doi.org/10.1093/molbev/msv274.
Swindell, W.R., & Bouzat, J.L. (2006). Selection and inbreeding depression: effects of inbreeding rate and inbreeding environment. Evolution, 60, 1014-1022.
Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585–595.
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 Biophysica Acta, 1308, 164–168. https://doi.org/10.1016/0167-4781(96)00100-5.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729. https://doi.org/10.1093/molbev/mst197.
Theodorou, K. & Couvet, D. (2006). On the expected relationship between inbreeding, fitness and extinction. Genetics Selection and Evolution, 38, 371-387. https://doi.org/10.1186/1297-9686-38-4-371.
Thompson, J.D., Higgins, D.G., & Gibson, T.J. (1994). Clustal W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680. https://doi.org/10.1093/nar/22.22.4673.
Van Grouw, H. (2013). What colour is that bird? The causes and recognition of common colour aberrations in birds. British Birds, 106, 17–29.
Vitalis, R., Dawson, K., & Boursot, P. (2001). Interpretation of variation across marker loci as evidence of selection. Genetics, 158, 1811–1823.
Vogel, F. (1972). Non-randomness of base replacement in point mutation. Journal of Molecular Evolution, 1, 334–367. https://doi.org/10.1007/BF01653962.
Wakeley, J. (1996). The excess of transitions among nucleotide substitutions: New methods of estimating transition bias underscore its significance. Trends in Ecological Evolution, 11, 158-162. https://doi.org/10.1016/0169-5347(96)10009-4.
Xu, Y., Liu, K., Han, Y., Xing, Y., Zhang, Y., Yang, Q., & Zhou, M. (2021). Codon usage bias regulates gene expression and protein conformation in yeast expression system P. pastoris. Microbial Cell Factories, 20, 91. https://doi.org/10.1186/s12934-021-01580-9.
Yakubu, A., Abimiku, H.K., Musa-Azara, I.S., Idahor, K.O., & Akinsola, O.M. (2013). Assessment of flock structure, preference in selection and traits of economic importance for domestic turkey (Meleagris gallopavo) genetic resources in Nassarawa State, Nigeria. Livestock Research for Rural Development, 25, 18.
Zhou, H., Wang, H., Huang, L.F., Naylor, M., & Clifford, P. (2005). Heterogeneity in codon usages of sobemovirus genes. Archives of Virology, 150, 1591–1605. https://doi.org/10.1007/s00705-005-0510-4.
Zou, Z., & Zhang, J. (2020). Are nonsynonymous transversions generally more deleterious than nonsynonymous transitions? Molecular Biology and Evolution, 38(1), 181-191. https://doi.org/10.1093/molbev/msaa200.
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The authors are grateful to turkey farmers in the southwest region of Nigeria for allowing us to take blood samples from their birds.
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S.O. Durosaro was involved in conceptualization, investigation, data collection, data analysis and manuscript writing. B.M. Ilori was involved in data collection, data analysis and manuscript writing. O.S. Iyasere was involved in investigation, data collection and manuscript writing. O.G. George was involved in investigation and data collection. O.A. Adewumi was involved in investigation and data collection. P.A. Ojo was involved in investigation and data collection. T.A. Yusuff was involved in investigation and data collection. M.R. Adetifa was involved in investigation and data collection. T.S. Atanda was involved in investigation and data collection. M.O. Ozoje was involved in investigation and manuscript writing.
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The protocol for the experiment was approved by Animal Care and Use Committee of College of Animal Science and Livestock Production of the Federal University of Agriculture, Abeokuta, Ogun State, Nigeria.
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Durosaro, S.O., Ilori, B.M., Iyasere, O.S. et al. Selection signatures in melanocortin-1 receptor gene of turkeys (Meleagris gallopavo) raised in hot humid tropics. Trop Anim Health Prod 54, 183 (2022). https://doi.org/10.1007/s11250-022-03185-9
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DOI: https://doi.org/10.1007/s11250-022-03185-9