Progress on the formation mechanism of sexual dimorphism plumage color in birds
Received date: 2022-01-04
Revised date: 2022-04-10
Online published: 2022-05-30
Supported by
Supported by the Sichuan Youth Science and Technology Fund No(2021JDJQ0008);the National Natural Science Foundation of China(31872345);the National Natural Science Foundation of China(32072703)
Sexually dimorphic plumage coloration is widespread in birds in which the male plumage is brighter than the female. This phenomenon is related to the environmental constraints on sexual selection or intraspecific competition between males and females in birds. The physiological factors and genetic regulation mechanism affecting the color of sexual dimorphism plumages in birds have always attracted significant attention in research. Understanding the diversity of sexually dimorphic traits provides insights into the mating strategies of the sexes and their behavior, ecology, and evolution. Interestingly, the ASIP, MC1R, TYRP1, and BCO2 genes have been identified to play a potential role in the coloration of melanin and carotenoids in bird sexual dimorphism plumages, either by controlling the rate and type of melanin or carotene synthesis or degradation by exerting an effect on the pigment biosynthetic pathway. In this review, we systematically summarize the biological significance, the direct causes (chemical and physical color), and the influence of sex hormones in sexually dimorphic plumage coloration. We also investigate the molecular mechanism underlying the roles of some genes on sexual dimorphism coloration, thereby providing a reference for in-depth understanding on the formation mechanism(s) of sexual dimorphic coloration in birds.
Key words: birds; plumage color; sex dimorphism
Jianmei Wang, Hehe Liu, Shengchao Ma, Yang Xi, Rongping Zhang, Qian Xu, Liang Li . Progress on the formation mechanism of sexual dimorphism plumage color in birds[J]. Hereditas(Beijing), 2022 , 44(6) : 491 -500 . DOI: 10.16288/j.yczz.22-004
| [1] | Hernández-Palma A. Light matters: testing the "Light Environment Hypothesis" under intra- and interspecific contexts. Ecol Evol, 2016, 6(12):4018-4031. |
| [2] | Cuthill IC, Allen WL, Arbuckle K, Caspers B, Chaplin G, Hauber ME, Hill GE, Jablonski NG, Jiggins CD, Kelber A, Mappes J, Marshall J, Merrill R, Osorio D, Prum R, Roberts NW, Roulin A, Rowland HM, Sherratt TN, Skelhorn J, Speed MP, Stevens M, Stoddard MC, Stuart-Fox D, Talas L, Tibbetts E, Caro T. The biology of color. Science, 2017, 357(6350):470. |
| [3] | Leinonen H, Tanila H. Vision in laboratory rodents-tools to measure it and implications for behavioral research. Behav Brain Res, 2018, 352:172-182. |
| [4] | Zuk M, Thornhill R, Ligon JD, Johnson K. Parasites and mate choice in red jungle fowl. Am Zool, 2015, 30(2):235-244. |
| [5] | Jones AG, Ratterman NL. Mate choice and sexual selection: what have we learned since Darwin? Proc Natl Acad Sci USA, 2009, 106(Suppl 1):10001-10008. |
| [6] | Zann RA. The Zebra Finch: A Synthesis of Field and Laboratory Studies. New York: Oxford University Press, 1996. |
| [7] | Laporte M, Berrebi P, Claude J, Vinyoles D, Pou-Rovira Q, Raymond JC, Magnan P. The ecology of sexual dimorphism in size and shape of the freshwater blenny salaria fluviatilis. Curr Zool, 2018, 64(2):183-191. |
| [8] | Andersson M, Iwasa Y. Sexual selection. Trends Ecol Evol, 1996, 11(2):53-58. |
| [9] | Payne RB. Sexual selection, lek and arena behavior, and sexual size dimorphism in birds. Ornithological Monographs, 1984(33):1-52. |
| [10] | Webster MS. Sexual dimorphism, mating system and body size in new world blackbirds (Icterinae). Evolution, 1992, 46(6):1621-1641. |
| [11] | Winquist T, Lemon RE. Sexual selection and exaggerated male tail length in birds. Am Nat, 1994, 143(1):95-116. |
| [12] | Zuk M, Thornhill R, Ligon JD, Johnson K, Austad S, Ligon SH, Thornhill NW, Costin C. The role of male ornaments and courtship behavior in female mate choice of red jungle fowl. Am Nat, 1990, 136(4):459-473. |
| [13] | Prost S, Armstrong EE, Nylander J, Thomas GWC, Suh A, Petersen B, Dalen L, Benz BW, Blom MPK, Palkopoulou E, Ericson PGP, Irestedt M. Comparative analyses identify genomic features potentially involved in the evolution of birds-of-paradise. Gigascience, 2019, 8(5): giz003. |
| [14] | Roulin A, Ducrest AL. Genetics of colouration in birds. Semin Cell Dev Biol, 2013, 24(6-7):594-608. |
| [15] | Hiyama G, Mizushima S, Matsuzaki M, Tobari Y, Choi JH, Ono T, Tsudzuki M, Makino S, Tamiya G, Tsukahara N, Sugita S, Sasanami T. Female Japanese quail visually differentiate testosterone-dependent male attractiveness for mating preferences. Sci Rep, 2018, 8(1):10012. |
| [16] | Sramkoski LL, McLaughlin WN,Cooley AM,Yuan DC,John A,Wittkopp PJ. Genetic architecture of a body colour cline in drosophila americana. Mol Ecol, 2020, 29(15):2840-2854. |
| [17] | Galván I, Solano F. Bird integumentary melanins: biosynthesis, forms, function and evolution. Int J Mol Sci, 2016, 17(4):520. |
| [18] | Haase E, Ito S, Wakamatsu K. Influences of sex, castration, and androgens on the eumelanin and pheomelanin contents of different feathers in wild mallards. Pigment Cell Res, 1995, 8(3):164-170. |
| [19] | Saino N, Romano M, Rubolini D, Teplitsky C, Ambrosini R, Caprioli M, Canova L, Wakamatsu K. Sexual dimorphism in melanin pigmentation, feather coloration and its heritability in the barn swallow (Hirundo rustica). PLoS One, 2013, 8(2):e58024. |
| [20] | Blount JD, Mcgraw KJ. Signal functions of carotenoid colouration. Carotenoids, 2008, 4:213-236. |
| [21] | Bramley PM. The biochemistry of the carotenoids. Volume 1: Plants (Second edition). Biochem Soc Trans, 1981, 9(5):484-485. |
| [22] | Delhey K, Roberts ML, Peters A. The carotenoid- continuum: carotenoid-based plumage ranges from conspicuous to cryptic and back again. BMC Ecol, 2010, 10:13. |
| [23] | Walker LK, Ewen JG, Brekke P, Kilner RM. Sexually selected dichromatism in the hihi notiomystis cincta: multiple colours for multiple receivers. J Evol Biol, 2014, 27(8):1522-1535. |
| [24] | Aguilera E, Amat JA. Carotenoids, immune response and the expression of sexual ornaments in male greenfinches (Carduelis chloris). Naturwissenschaften, 2007, 94(11):895-902. |
| [25] | Albéric M, Dean MN, Gourrier A, Wagermaier W, Dunlop JWC, Staude A, Fratzl P, Reiche I. Relation between the macroscopic pattern of elephant ivory and its three- dimensional micro-tubular network. PLoS One, 2017, 12(1):e0166671. |
| [26] | Kohri M. Progress in polydopamine-based melanin mimetic materials for structural color generation. Sci Technol Adv Mater, 2021, 21(1), 833-848. |
| [27] | Durrer H, Villiger W. Schillerfarben der trogoniden. J Ornithol, 1966, 107(1):1-26. |
| [28] | Giraldo MA, Parra JL, Stavenga DG. Iridescent colouration of male anna's hummingbird (Calypte anna) caused by multilayered barbules. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 2018, 204(12):965-975. |
| [29] | Schmidt WJ, Ruska H. Über das schillernde federmelanin bei heliangelus und lophophorus. Zeitschrift für Zellforschung und Mikroskopische Anatomie, 1962, 57(1):1-36. |
| [30] | Rutschke E. Die submikroskopische struktur schillernder federn von entenvögeln. Zeitschrift für Zellforschung und Mikroskopische Anatomie, 2004, 73:432-443. |
| [31] | Shawkey MD, Estes AM, Siefferman L, Hill GE. The anatomical basis of sexual dichromatism in non-iridescent ultraviolet-blue structural coloration of feathers. Biol J Linn Soc, 2005, 84(2):259-271. |
| [32] | Eliason CM, Shawkey MD. A photonic heterostructure produces diverse iridescent colours in duck wing patches. J R Soc Interface, 2012, 9(74):2279-2289. |
| [33] | Fox DL. Animal Biochromes and Structural Colours: Physical, Chemical, Distribution & Physiological Features of Coloured Bodies in the Animal World. New York: University of California Press, 1976. |
| [34] | Khudiyev T, Dogan T, Bayindir M. Biomimicry of multifunctional nanostructures in the neck feathers of mallard (Anas platyrhynchos L.) drakes. Sci Rep, 2014, 4:4718. |
| [35] | Ma SC, Liu HH, Wang JM, Wang L, Xi Y, Liu YS, Xu Q, Hu JW, Han CC, Bai LL, Li L, Wang JW. Transcriptome analysis reveals genes associated with sexual dichromatism of head feather color in mallard. Front Genet, 2021, 12:627974. |
| [36] | Lee E, Aoyama M, Sugita S. Microstructure of the feather in japanese jungle crows (Corvus macrorhynchos) with distinguishing gender differences. Anat Sci Int, 2009, 84(3):141-147. |
| [37] | Adkins-Regan E. Hormones and Animal Social Behavior. Princeton: Princeton University Press, 2013. |
| [38] | Hearing VJ, Tsukamoto K. Enzymatic control of pigmentation in mammals. FASEB J, 1991, 5(14):2902-2909. |
| [39] | Jimbow K, Alena F, Dixon W, Hara H. Regulatory factors of pheo-and eumelanogenesis in melanogenic compartments. Pigment Cell Res, 1992, Suppl 2: 36-42. |
| [40] | Kimball RT, Ligon JD. Evolution of avian plumage dichromatism from a proximate perspective. Am Nat, 1999, 154(2):182-193. |
| [41] | Owens IP, Short RV. Hormonal basis of sexual dimorphism in birds: implications for new theories of sexual selection. Trends Ecol Evol, 1995, 10(1):44-47. |
| [42] | Lorin T, Salzburger W, Böhne A. Evolutionary fate of the androgen receptor-signaling pathway in ray-finned fishes with a special focus on cichlids. G3 (Bethesda), 2015, 5(11):2275-2283. |
| [43] | Siefferman L, Liu M, Navara KJ, Mendonça MT, Hill GE. Effect of prenatal and natal administration of testosterone on production of structurally based plumage coloration. Physiol Biochem Zool, 2013, 86(3):323-332. |
| [44] | Van Oordt GJ, Bruyns MFM. studien über die gonaden übersommernder vögel. IV. Die gonaden übersommernder austernfischer. (Haematopus ostralegus L.). Zeitschrift für Morphologie und Ökologie der Tiere, 1938, 34(2):161-172. |
| [45] | McGlothlin JW, Jawor JM, Greives TJ, Casto JM, Phillips JL, Ketterson ED. Hormones and honest signals: males with larger ornaments elevate testosterone more when challenged. J Evol Biol, 2008, 21(1):39-48. |
| [46] | Lindsay WR, Webster MS, Varian CW, Schwabl H. Plumage colour acquisition and behaviour are associated with androgens in a phenotypically plastic tropical bird. Anim Behav, 2009, 77(6):1525-1532. |
| [47] | Khalil S, Welklin JF, McGraw KJ,Boersma J,Schwabl H,Webster MS,Karubian J. Testosterone regulates CYP2J19- linked carotenoid signal expression in male red-backed fairywrens (Malurus melanocephalus). Proc Biol Sci, 2020, 287(1935):20201687. |
| [48] | Chen CF, Foley J, Tang PC, Li A, Jiang TX, Wu P, Widelitz RB, Chuong CM. Development, regeneration, and evolution of feathers. Annu Rev Anim Biosci, 2015, 3:169-195. |
| [49] | Boersma J, Jones JA, Enbody ED, Welklin JF, Ketaloya S, Karubian J, Schwabl H. Male white-shouldered fairywrens (Malurus alboscapulatus) elevate testosterone when courting females but not during territorial challenges. bioRxiv, 2021, 142:105158. |
| [50] | Lindsay WR, Webster MS, Schwabl H. Sexually selected male plumage color is testosterone dependent in a tropical passerine bird, the red-backed fairy-wren (Malurus melanocephalus). PLoS One, 2011, 6(10):e26067. |
| [51] | Lantz SM, Boersma J, Schwabl H, Karubian J. Early-moulting red-backed fairywren males acquire ornamented plumage in the absence of elevated androgens. Emu Austral Ornithol, 2017, 117(2):170-180. |
| [52] | Gluckman TL, Mundy NI. Evolutionary pathways to convergence in plumage patterns. BMC Evol Biol, 2016, 16(1):172. |
| [53] | Bókony V, Garamszegi LZ, Hirschenhauser K, Liker A. Testosterone and melanin-based black plumage coloration: a comparative study. Behav Ecol Sociobiology, 2008, 62(8):1229. |
| [54] | Boersma J, Enbody ED, Jones JA, Nason D, Lopez- Contreras E, Karubian J, Schwabl H. Testosterone induces plumage ornamentation followed by enhanced territoriality in a female songbird. Behav Ecol, 2020, 31(5):1233-1241. |
| [55] | Trigo S, Mota PG. A test of the effect of testosterone on a sexually selected carotenoid trait in a cardueline finch. Ecol Res, 2015, 30(1):25-31. |
| [56] | Mueller NS. An experimental study of sexual dichromatism in the duck Anas platyrhynchos. J Exp Zool, 1970, 173(3):263-268. |
| [57] | Keck WN. The control of the secondary sex characters in the English sparrow, passer domesticus (Linnaeus). J Exp Zool, 1934, 67(2):315-347. |
| [58] | Yu FF, Qu BL, Lin DD, Deng YW, Huang RL, Zhong ZM. Pax3 gene regulated melanin synthesis by tyrosinase pathway in pteria penguin. Int J Mol Sci, 2018, 19(12):3700. |
| [59] | Liu XX, Du B, Zhang PQ, Zhang JZ, Zhu ZW, Liu B, Fan RW. miR-380-3p regulates melanogenesis by targeting SOX6 in melanocytes from alpacas (Vicugna pacos). BMC Genomics, 2019, 20(1):962. |
| [60] | Ran JS, You XY, Jin J, Zhou YG, Wang Y, Lan D, Ren P, Liu YP. The relationship between MC1R mutation and plumage color variation in pigeons. Biomed Res Int, 2016, 2016:3059756. |
| [61] | San-Jose LM, Ducrest AL, Ducret V, Béziers P, Simon C, Wakamatsu K, Roulin A. Effect of the MC1R gene on sexual dimorphism in melanin-based colorations. Mol Ecol, 2015, 24(11):2794-2808. |
| [62] | Zhang J, Liu Y, Liu AF. Progress of candidate genes ASIP and TYRP1 for plumage color in animal. China Poult, 2015, 37(1):55-58. |
| [62] | 张静, 刘毅, 刘安芳. 畜禽羽色候选基因ASIP和TYRP1的研究进展. 中国家禽, 2015, 37(1):55-58. |
| [63] | Oribe E, Fukao A, Yoshihara C, Mendori M, Rosal KG, Takahashi S, Takeuchi S. Conserved distal promoter of the agouti signaling protein (ASIP) gene controls sexual dichromatism in chickens. Gen Comp Endocrinol, 2012, 177(2):231-237. |
| [64] | Melamed E, Arnold AP. Regional differences in dosage compensation on the chicken Z chromosome. Genome Biol, 2007, 8(9):R202. |
| [65] | Kuroiwa A. Sex-determining mechanism in avians. Adv Exp Med Biol, 2017, 1001:19-31. |
| [66] | Wang JM, Xi Y, Ma SC, Qi JJ, Li JP, Zhang RP, Han CC, Li L, Wang JW, Liu HH. Single-molecule long-read sequencing reveals the potential impact of posttranscriptional regulation on gene dosage effects on the avian Z chromosome. BMC Genomics, 2022, 23(1):122. |
| [67] | Gazda MA, Araújo PM, Lopes RJ, Toomey MB, Andrade P, Afonso S, Marques C, Nunes L, Pereira P, Trigo S, Hill GE, Corbo JC, Carneiro M. A genetic mechanism for sexual dichromatism in birds. Science, 2020, 368(6496):1270-1274. |
| [68] | Gibson WB. The nature of animal colours. JAMA, 1961, 84(4):708-709. |
| [69] | McGraw KJ, Hill GE, Stradi R, Parker RS. The effect of dietary carotenoid access on sexual dichromatism and plumage pigment composition in the american goldfinch. Comp Biochem Physiol B Biochem Mol Biol, 2002, 131(2):261-269. |
| [70] | Yang Y, Wu LN, Chen JF, Wu X, Xia JH, Meng ZN, Liu XC, Lin HR. Whole-genome sequencing of leopard coral grouper (Plectropomus leopardus) and exploration of regulation mechanism of skin color and adaptive evolution. Zool Res, 2020, 41(3):328-340. |
| [71] | Price TD. Sensory drive, color, and color vision. Am Nat, 2017, 190(2):157-170. |
| [72] | Osorio D, Vorobyev M. A review of the evolution of animal colour vision and visual communication signals. Vision Res, 2008, 48(20):2042-2051. |
| [73] | Price-Waldman R, Stoddard MC. Avian coloration genetics: recent advances and emerging questions. J Hered, 2021, 112(5):395-416. |
| [74] | Lemaire BS. No evidence of spontaneous preference for slowly moving objects in visually naïve chicks. Sci Rep, 2020, 10(1):6277. |
/
| 〈 |
|
〉 |