Scales in the Early Cretaceous bird <em>Gansus</em> from China provide evidence on the evolution of avian scales

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Abstract

Most modern birds have scales covering feet, but our knowledge of early avian scales is limited, mainly due to their scarcity in the fossil record. Here we describe the morphological details of scutellate and interstitial scales preserved in IVPP V15077, a specimen of the Early Cretaceous bird Gansus from the Changma Basin in northwestern Gansu Province, Northwest China. These results, combined with previous reports of scutate and reticulate scales, show that all four types of scales present in modern birds already appeared in the Early Cretaceous. The phylogenetic distribution of skin appendages of feet, including feathers and scales, shows that non-avian dinosaurs already evolved scales resembling those in modern birds, and that scales can coexist with feathers on feet, suggesting that avian scales may be homologue with scales of non-avian dinosaurs. However, to further test this hypothesis, more research combined with a strengthened focus on detecting specimens with soft tissue preservation is necessary.

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Key words: Foot scale Avian scale Feather Bird Dinosaur Changma Basin Early Cretaceous

Received: 22 December 2021

Corresponding Authors: * E-mail address: panyanhong@nju.edu.cn (Y.-H. Pan).

Cite this article:

. Scales in the Early Cretaceous bird Gansus from China provide evidence on the evolution of avian scales[J]. Journal of Palaeogeography, 2022, 11(4): 640-652.

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http://journal09.magtechjournal.com/Jweb_jop/EN/10.1016/j.jop.2022.08.002 OR http://journal09.magtechjournal.com/Jweb_jop/EN/Y2022/V11/I4/640

[1] Anderson R.P., Tosca N.J., Gaines R.R., Koch N.M., Briggs D.E.G., 2018. A mineralogical signature for Burgess Shale-type fossilization. Geology, 46, 347-350. https://doi.org/10.1130/G39941.1.
[2] Bartels T.,2003. Variations in the morphology, distribution, and arrangement of feathers in domesticated birds.
[3] Journal of Experimental Zoology B: Molecular and Developmental Evolution, 298(1), 91-108. https://doi.org/10.1002/jez.b.28.
[4] Boer E.F.,Van Hollebeke, H.F., Shapiro, M.D., 2017. Genomic determinants of epidermal appendage patterning and structure in domestic birds. Developmental Biology, 429, 409-419. https://doi.org/10.1016/j.ydbio.2017.03.022.
[5] Bortoluzzi C., Megens H.J., Bosse M., Derks M.F.L., Dibbits B., Laport K., Weigend S., Groenen M.A.M., Crooijmans R.P.M.A., 2020. Parallel genetic origin of foot feathering in birds. Molecular Biology and Evolution, 37, 2465-2476. https://doi.org/10.1093/molbev/msaa092.
[6] Briggs D.E.G., Kear A.J., 1993. Decay and preservation of polychaetes: Taphonomic thresholds in soft-bodied organisms. Paleobiology, 19, 107-135. https://doi.org/10.1017/S0094837300012343.
[7] Brush A.H.,1985. Convergent evolution of reticulate scales. Journal of Experimental Zoology, 236, 303-308. https://doi.org/10.1002/jez.1402360307.
[8] Clarke J.A.,2004. Morphology, phylogenetic taxonomy, and systematics of Ichthyornis and Apatornis (Avialae: Ornithurae). Bulletin of the American Museum of Natural History, 2004, 1-179. https://doi.org/10.1206/0003-0090(2004)286<0001:MPTASO>2.0.CO;2.
[9] Colleary C., Dolocan A., Gardner J., Singh S., Wuttke M., Rabenstein R., Habersetzer J., Schaal S., Feseha M., Clemens M., Jacobs B.F., Currano E.D., Jacobs L.L., Sylvestersen R.L., Gabbott S.E., Vinther J., 2015. Chemical, experimental, and morphological evidence for diagenetically altered melanin in exceptionally preserved fossils. Proceedings of the National Academy of Sciences, 112, 12592. https://doi.org/10.1073/pnas.150 9831112.
[10] Cuesta E.,Díaz-Martínez, I., Ortega, F., Sanz, J.L., 2015. Did all theropods have chicken-like feet? First evidence of a non-avian dinosaur podotheca. Cretaceous Research, 56, 53-59. https://doi.org/10.1016/j.cretres.2015.03.008.
[11] Dhouailly D.,2009. A new scenario for the evolutionary origin of hair, feather, and avian scales. Journal of Anatomy, 214, 587-606. https://doi.org/10.1111/j.1469-7580.2008.01041.x.
[12] Di-Poï N., Milinkovitch M.C., 2016. The anatomical placode in reptile scale morphogenesis indicates shared ancestry among skin appendages in amniotes. Science Advances, 2, e1600708. https://doi.org/10.1126/sciadv.1600708.
[13] Domyan E.T., Kronenberg Z., Infante C.R., Vickrey A.I., Stringham S.A., Bruders R., Guernsey M.W., Park S., Payne J., Beckstead R.B., Kardon G., Menke D.B., Yandell M., Shapiro M.D., 2016. Molecular shifts in limb identity underlie development of feathered feet in two domestic avian species. Elife, 5, e12115. https://doi.org/10.7554/eLife.12115.
[14] Falk A.R., Kaye T.G., Zhou Z., Burnham D.A., 2016. Laser ﬂuorescence illuminates the soft tissue and life habits of the Early Cretaceous bird Confuciusornis. PLoS ONE, 11, e0167284. https://doi.org/10.1371/journal.pone.0167284.
[15] Feduccia A.,1993. Evidence from claw geometry indicating arboreal habits of Archaeopteryx. Science, 259, 790-793. https://doi.org/10.1126/science.259.5096.790.
[16] Foth C., Tischlinger H., Rauhut O.W.M., 2014. New specimen of Archaeopteryx provides insights into the evolution of pennaceous feathers. Nature, 511, 79-82. https://doi.org/10.1038/nature13467.
[17] Galton P.M., Martin L.D., 2002. Postcranial anatomy and systematics of Enaliornis Seeley, 1876, a foot-propelled diving bird (Aves: Ornithurae: Hesperornithiformes) from the Early Cretaceous of England. Revue de Paleobiologie, 21, 489-538.
[18] Godefroit P., Sinitsa S.M., Cincotta A., McNamara, M.E., Reshetova, S.A., Dhouailly, D., 2020. Integumentary structures in Kulindadromeus zabaikalicus, a basal neornithischian dinosaur from the Jurassic of Siberia. In: The Evolution of Feathers. Springer, pp. 47-65.
[19] Godefroit P., Sinitsa S.M., Dhouailly D., Bolotsky Y.L., Sizov A.V., McNamara M.E., Benton M.J., Spagna P., 2014. A Jurassic ornithischian dinosaur from Siberia with both feathers and scales. Science, 345, 451-455.
[20] Greenwold M.J., Sawyer R.H., 2013. Molecular evolution and expression of archosaurian β-keratins: Diversiﬁcation and expansion of archosaurian β-keratins and the origin of feather β-keratins. Journal of Experimental Zoology B: Molecular and Developmental Evolution, 320, 393-405. https://doi.org/10.1002/jez.b.22514 https://doi.org/.
[21] Hendrickx C., Bell P.R., Pittman M., Milner A.R.C., Cuesta E., O'Connor J., Loewen M., Currie P.J., Mateus O., Kaye T.G., Delcourt R., 2022. Morphology and distribution of scales, dermal ossiﬁcations, and other non-feather integumentary structures in non-avialan theropod dinosaurs. Biological Reviews, 97, 960-1004. https://doi.org/10.1111/brv.12829.
[22] Hohn E.,1977. The “snowshoe effect” of the feathering on ptarmigan feet. The Condor, 79, 380-382.
[23] Holthaus K.B., Eckhart L., Dalla Valle L., Alibardi L., 2019. Review: Evolution and diversiﬁcation of corneous beta-proteins, the characteristic epidermal proteins of reptiles and birds. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 330, 438-453. https://doi.org/10.1002/jez.b.22840 https://doi.org/.
[24] Homberger D.G., Brush A.H., 1986. Functional-morphological and biochemical correlations of the keratinized structures in the African Grey Parrot, Psittacus erithacus (Aves). Zoomorphology, 106, 103-114.
[25] Hou L., Liu Z., 1984. A new fossil bird from Lower Cretaceous of Gansu and early evolution of birds. Scientia Sinica (Series B), 27(12), 1296-1303.
[26] Hu D., Hou L., Zhang L., Xu X., 2009. A pre-Archaeopteryx troodontid theropod from China with long feathers on the metatarsus. Nature, 461, 640-643. https://doi.org/10.1038/nature08322.
[27] Ji S., Ji Q., You H., Lü J., Yuan C., 2006. Webbed foot of an Early Cretaceous ornithurine bird Gansus from China. Geological Bulletin of China, 25(11), 1295-1298.
[28] Ji S.A., Ji Q., Lü J., Yuan C.X., 2007. A new giant compsognathid dinosaur with long ﬁlamentous integuments from Lower Cretaceous of Northeastern China. Acta Geologica Sinica (English Edition), 81, 8-15.
[29] Kelso L., Kelso E.H., 1936. The relation of feathering of feet of American owls to humidity of environment and to life zones. The Auk, 53, 51-56. https://doi.org/10.2307/4077355.
[30] Li Q., Gao K.Q., Meng Q., Clarke J.A., Shawkey M.D., D'Alba L., Pei R., Ellison M., Norell M.A., Vinther J., 2012. Reconstruction of Microraptor and the evolution of iridescent plumage. Science, 335, 1215-1219. https://doi.org/10.1126/science.1213780.
[31] Li Q., Gao K.Q., Vinther J., Shawkey M.D., Clarke J.A., D'Alba L., Meng Q., Briggs D.E.G., Prum R.O., 2010. Plumage color patterns of an extinct dinosaur. Science, 327, 1369-1372. https://doi.org/10.1126/science.1186 290.
[32] Li Y., Zhang Y., Zhou Z., Li Z., Liu D., Wang X., 2011. New material of Gansus and a discussion on its habit. Vertebrata PalAsiatica, 49, 435-445.
[33] Lindgren J., Everhart M.J., Caldwell M.W., 2011. Three-dimensionally preserved integument reveals hydrodynamic adaptations in the extinct marine lizard Ectenosaurus (Reptilia, Mosasauridae). PLoS ONE, 6(11), e27343. https://doi.org/10.1371/journal.pone.0027343.
[34] Lucas A.M., Stettenheim P.R., 1972. Avian Anatomy: Integument. US Agricultural Research Service. D.C, Washington.
[35] McNamara, M.E., Orr, P.J., Kearns, S.L., Alcala, L., Anadon, P., Penalver, E., 2016. Reconstructing carotenoid-based and structural coloration in fossil skin. Current Biology, 26, 1075-1082. https://doi.org/10.1016/j.cub.2016.02.038.
[36] McNamara, M.E., Orr, P.J., Kearns, S.L., Alcala, L., Anadon, P., Penalver Molla, E., 2009. Soft-tissue preservation in Miocene frogs from Libros, Spain: Insights into the genesis of decay microenvironments. PALAIOS, 24, 104-117. https://doi.org/10.2110/palo.2008.p08-017r.
[37] McNamara M.E., Zhang F., Kearns S.L., Orr P.J., Toulouse A., Foley T., Hone D.W.E., Rogers C.S., Benton M.J., Johnson D., Xu X., Zhou Z., 2018. Fossilized skin reveals coevolution with feathers and metabolism in feathered dinosaurs and early birds. Nature Communications, 9, 2072. https://doi.org/10.1038/s41467-018-04443-x.
[38] Naimark E., Kalinina M., Shokurov A., Boeva N., Markov A., Zaytseva L., 2016. Decaying in different clays: Implications for soft-tissue preservation. Palaeontology, 59, 583-595. https://doi.org/10.1111/pala.12246.
[39] Naimark E., Kalinina M., Shokurov A., Markov A., Zaytseva L., Boeva N., 2018. Mineral composition of host sediments inﬂuences the fossilization of soft tissues. Canadian Journal of Earth Sciences, 55, 1271-1283. https://doi.org/10.1139/cjes-2017-0237.
[40] O'Connor J., Zhou Z., Xu X., 2011. Additional specimen of Microraptor provides unique evidence of dinosaurs preying on birds. Proceedings of the National Academy of Sciences, 108, 19662-19665. https://doi.org/10.1073/pnas.1117727108.
[41] Petrovich R.,2001. Mechanisms of fossilization of the soft-bodied and lightly armored faunas of the Burgess Shale and of some other classical localities. American Journal of Science, 301, 683-726. https://doi.org/10.2475/ajs.301.8.683.
[42] Prin F., Dhouailly D., 2004. How and when the regional competence of chick epidermis is established: Feathers vs. scutate and reticulate scales, a problem en route to a solution. International Journal of Developmental Biology, 48, 137-148. https://doi.org/10.1387/ijdb.15272378.
[43] Pu H., Chang H., Lü J., Wu Y., Xu L., Zhang J., Jia S., 2013. A new juvenile specimen of Sapeornis (Pygostylia: Aves) from the Lower Cretaceous of Northeast China and allometric scaling of this basal bird. Paleontological Research, 17, 27-38. https://doi.org/10.2517/1342-8144-17.1.27.
[44] Rossi V., McNamara M.E., Webb S.M., Ito S., Wakamatsu K., 2019. Tissue-speciﬁc geometry and chemistry of modern and fossilized melanosomes reveal internal anatomy of extinct vertebrates. Proceedings of the National Academy of Sciences, 116(36), 17880-17889. https://doi.org/10.1073/pnas.1820285116.
[45] Sagemann J., Bale S.J., Briggs D.E.G., Parkes R.J., 1999. Controls on the formation of authigenic minerals in association with decaying organic matter: An experimental approach. Geochimica et Cosmochimica Acta, 63, 1083-1095. https://doi.org/10.1016/S0016-7037(99) 00087-3.
[46] Sawyer R.H., Knapp L.W., O'Guin, W.M., 1986. Epidermis, dermis and appendages. In: Biology of the Integument. Springer, pp. 194-238.
[47] Suarez M.B., Ludvigson G.A., Gonzalez L.A., Al-Suwaidi A.H., You H.L., 2013. Stable isotope chemostratigraphy in lacustrine strata of the Xiagou Formation, Gansu Province, NW China. Geological Society, London, Special Publications, 382, 143-155. https://doi.org/10.1144/SP382.1.
[48] Suarez M.B., Ludvigson G.A., Gonzalez L.A., You H.L.,2017. Continental paleotemperatures from an Early Cretaceous dolomitic lake, Gansu Province, China. Journal of Sedimentary Research, 87, 486-499. https://doi.org/10.2110/jsr.2017.31.
[49] Vinther, J., Briggs, D.E.G., Prum, R.O., Saranathan, V., 2008. The colour of fossil feathers. Biology Letters, 4, 522-525. https://doi.org/10.1098/rsbl.2008.0302.
[50] Vinther J., Nicholls R., Lautenschlager S., Pittman M., Kaye T.G., Rayﬁeld E., Mayr G., Cuthill I.C.,2016. 3D Camouﬂage in an ornithischian dinosaur. Current Biology, 26, 2456-2462. https://doi.org/10.1016/j.cub.2016.06.065.
[51] Wang B., Yang W.,McKittrick, J., Meyers, M.A., 2016. Keratin: Structure, mechanical properties, occurrence in biological organisms, and efforts at bioinspiration. Progress in Materials Science, 76, 229-318. https://doi.org/10.1016/j.pmatsci.2015.06.001.
[52] Wang M., Zheng X., O'Connor J.K., Lloyd G.T., Wang X., Wang Y., Zhang X., Zhou Z., 2015. The oldest record of Ornithuromorpha from the Early Cretaceous of China. Nature Communications, 6, 6987. https://doi.org/10.1038/ncomms7987.
[53] Wang M., Zhou Z., O'Connor J.K., Zelenkov N.V., 2014. A new diverse enantiornithine family (Bohaiornithidae fam. nov.) from the Lower Cretaceous of China with information from two new species. Vertebrata PalAsiatica, 52, 31-76.
[54] Wang X., Pittman M., Zheng X., Kaye T.G., Falk A.R., Hartman S.A., Xu X., 2017. Basal paravian functional anatomy illuminated by high-detail body outline. Nature Communications, 8, 14576. https://doi.org/10.1038/ncomms14576.
[55] Wilson L.A., Butterﬁeld N.J.,2014. Sediment effects on the preservation of Burgess Shale-type compression fossils. PALAIOS, 29, 145-154. https://doi.org/10.2110/palo.2013.075.
[56] Wu P., Lai Y.C., Widelitz R., Chuong C.M., 2018. Comprehensive molecular and cellular studies suggest avian scutate scales are secondarily derived from feathers, and more distant from reptilian scales. Scientiﬁc Reports, 8, 16766. https://doi.org/10.1038/s41598-018-35176-y.
[57] Xing L., McKellar R.C., O'Connor J.K., Bai M., Tseng K., Chiappe L.M., 2019a. A fully feathered enantiornithine foot and wing fragment preserved in mid-Cretaceous Burmese amber. Scientiﬁc Reports, 9, 927. https://doi.org/10.1038/s41598-018-37427-4.
[58] Xing L.,O'Connor, J.K., Chiappe, L.M., McKellar, R.C., Carroll, N., Hu, H., Bai, M., Lei, F., 2019b. A new enantiornithine bird with unusual pedal proportions found in amber. Current Biology, 29, 2396-2401. https://doi.org/10.1016/j.cub.2019.05.077.
[59] Xing L.,O'Connor, J.K., McKellar, R.C., Chiappe, L.M., Tseng, K., Li, G., Bai, M., 2017. A mid-Cretaceous enantiornithine (Aves) hatchling preserved in Burmese amber with unusual plumage. Gondwana Research, 49, 264-277. https://doi.org/10.1016/j.gr.2017.06.001.
[60] Xu X., Zhou Z., Dudley R., Mackem S., Chuong C.-M., Erickson G.M., Varricchio D.J., 2014. An integrative approach to understanding bird origins. Science, 346, 1253293. https://doi.org/10.1126/science.1253293.
[61] Xu X., Zhou Z., Wang X., Kuang X., Zhang F., Du X., 2003. Four-winged dinosaurs from China. Nature, 421, 335-340. https://doi.org/10.1038/nature01342.
[62] Xue P., Kuang H., Liu Y., Peng N., Wang X., Xu J., Liu H., Jiang X., 2013. Sedimentary facies of the Early Cretaceous Xiagou Formation and Zhonggou Formation and basin evolution in western Jiuquan, Gansu Province. Geological Bulletin of China, 32, 476-487.
[63] You H., Lamanna M.C., Harris J.D., Chiappe L.M., O'Connor J., Ji S., Lü J., Yuan C., Li D., Zhang X., Lacovara K.J., Dodson P., Ji Q., 2006. A nearly modern amphibious bird from the Early Cretaceous of northwestern China. Science, 312, 1640-1643. https://doi.org/10.1126/science.1126377.
[64] Zhang F., Kearns S.L., Orr P.J., Benton M.J., Zhou Z., Johnson D., Xu X., Wang X., 2010. Fossilized melanosomes and the colour of Cretaceous dinosaurs and birds. Nature, 463, 1075-1078. https://doi.org/10.1038/nature08740.
[65] Zheng X., Zhou Z., Wang X., Zhang F., Zhang X., Wang Y., Wei G., Wang S., Xu X., 2013. Hind wings in basal birds and the evolution of leg feathers. Science, 339, 1309-1312. https://doi.org/10.1126/science.1228753.
[66] Zhou Z.,2004. The origin and early evolution of birds: Discoveries, disputes, and perspectives from fossil evidence. Naturwissenschaften, 91, 455-471. https://doi.org/10.1007/s00114-004-0570-4.
[67] Zhou Z., Zhang F., 2005. Discovery of an ornithurine bird and its implication for Early Cretaceous avian radiation. Proceedings of the National Academy of Sciences, 102, 18998-19002. https://doi.org/10. 1073/pnas.0507106102.
[68] Zhu S., Cui H., Jia Y., Zhu X., Tong H., Ma L.,2020. Occurrence, composition, and origin of analcime in sedimentary rocks of non-marine petroliferous basins in China. Marine and Petroleum Geology, 113, 104164. https://doi.org/10.1016/j.marpetgeo.2019.104164.