Comparative digital reconstruction of Pica pica and Struthio camelus and their cranial suture ontogenies.

birds ontogeny osteology skull morphology

Journal

Anatomical record (Hoboken, N.J. : 2007)
ISSN: 1932-8494
Titre abrégé: Anat Rec (Hoboken)
Pays: United States
ID NLM: 101292775

Informations de publication

Date de publication:
Jan 2024
Historique:
revised: 25 05 2023
received: 01 02 2023
accepted: 26 05 2023
pubmed: 20 6 2023
medline: 20 6 2023
entrez: 20 6 2023
Statut: ppublish

Résumé

To date, several studies describe post-hatching ontogenetic variation in birds; however, none of these studies document and compare ontogenetic variation of the entire skull in multiple avian species. Therefore, we studied ontogenetic skull variation of two bird species with very different ecologies, Pica pica, and Struthio camelus, using μCT based 3D reconstructions. For each specimen, we performed bone-by-bone segmentation in order to visualize and describe the morphological variation of each bone during ontogeny and estimated the average sutural closure of the skulls to identify different ontogenetic stages. Although bone fusion of P. pica occurs more rapidly than that of S. camelus the general sequence of bone fusion follows a similar trend from posterior to anterior, but a more detailed analysis reveals some interspecific variation in the fusion patterns. Although growth persists over a longer period in S. camelus than in P. pica and adults of the former species are significantly larger, the skull of the most mature S. camelus is still less fused than that of P. pica. Different growth and fusion patterns of the two species indicate that the interspecific ontogenetic variation could be related to heterochronic developments. Nevertheless, this hypothesis needs to be tested in a broader phylogenetic framework in order to detect the evolutionary direction of the potential heterochronic transformations.

Identifiants

pubmed: 37338258
doi: 10.1002/ar.25275
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

5-48

Subventions

Organisme : New York Institute of Technology College of Osteopathic Medicine
Organisme : Oklahoma State University Center for Health Sciences
Organisme : Swiss National Science Fondation
ID : PZ00P2_174040
Organisme : U.S. National Science Foundation
ID : 1457180
Organisme : U.S. National Science Foundation
ID : 1725925
Organisme : University of Arizona
Organisme : Western Interior Paleontological Society

Informations de copyright

© 2023 The Authors. The Anatomical Record published by Wiley Periodicals LLC on behalf of American Association for Anatomy.

Références

Acosta Hospitaleche, C., Picasso, M. B., & Pérez, L. M. (2020). Integrative analysis of the quaternary avian remains from Última Esperanza, Chile. Journal of South American Earth Sciences, 102, 102673.
Alberch, P., Gould, S. J., Oster, G. F., & Wake, D. B. (1979). Size and shape in ontogeny and phylogeny. Paleobiology, 5, 296-317.
Arnaout, B., Lantigua, K. E., MacKenzie, E. M., McKinnell, I. W., & Maddin, H. C. (2021). Development of the chicken skull: A complement to the external staging table of hamburger and Hamilton. Anatomical Record, 304, 2726-2740.
Bailleul, A. M., Scannella, J. B., Horner, J. R., & Evans, D. C. (2016). Fusion patterns in the skulls of modern archosaurs reveal that sutures are ambiguous maturity indicators for the Dinosauria. PLoS One, 11, e0147687.
Balanoff, A. M., & Rowe, T. B. (2007). Osteological description of an embryonic skeleton of the extinct elephant bird, Aepyornis (palaeognathae: Ratitae). Journal of Vertebrate Paleontology, 27, 1-53.
Barrowclough, G. F., Cracraft, J., Klicka, J., & Zink, R. M. (2016). How many kinds of birds are there and why does it matter? PLoS One, 11, e0166307.
Baumel, J. J., & Witmer, L. M. (1993). Osteologia. In J. J. Baumel, A. S. King, J. E. Breazile, H. E. Evans, & J. C. vanden Berge (Eds.), Handbook of avian anatomy (pp. 45-132). Nuttall Ornithological Club.
Benson, R. B., Starmer-Jones, E., Close, R. A., & Walsh, S. A. (2017). Comparative analysis of vestibular ecomorphology in birds. Journal of Anatomy, 231, 990-1018.
Beyrand, V., Voeten, D. F., Bureš, S., Fernandez, V., Janáček, J., Jirák, D., Rauhut, O., & Tafforeau, P. (2019). Multiphase progenetic development shaped the brain of flying archosaurs. Scientific Reports, 9(10807), 1-15.
Bhullar, B. A. S., Marugán-Lobón, J., Racimo, F., Bever, G. S., Rowe, T. B., Norell, M. A., & Abzhanov, A. (2012). Birds have paedomorphic dinosaur skulls. Nature, 487, 223-226.
Böhmer, C., Prevoteau, J., Duriez, O., & Abourachid, A. (2020). Gulper, ripper and scrapper: Anatomy of the neck in three species of vultures. Journal of Anatomy, 236, 701-723.
Bunce, M., Worthy, T. H., Phillips, M. J., Holdaway, R. N., Willerslev, E., Haile, J., Shapiro, B., Scofield, R. P., Drummond, A., Kamp, P. J. J., & Cooper, A. (2009). The evolutionary history of the extinct ratite moa and New Zealand Neogene paleogeography. Proceedings of the National Academy of Sciences of the United States of America, 106, 1-6.
Cardini, A., & Polly, P. D. (2013). Larger mammals have longer faces because of size-related constraints on skull form. Nature Communications, 4(2458), 1-9.
Carril, J., & Tambussi, C. P. (2017). Skeletogenesis of Myiopsitta monachus (Psittaciformes) and sequence heterochronies in Aves. Evolution and Development, 19, 17-28.
Carril, J., Tambussi, C. P., & Rasskin-Gutman, D. (2021). The network ontogeny of the parrot: Altriciality, dynamic skeletal assemblages, and the avian body plan. Evolutionary Biology, 48, 41-53.
Cooper, R. G. (2005). Growth in the ostrich (Struthio camelus var. domesticus). Animal Science Journal, 76, 1-4.
Crole, M. R., & Soley, J. T. (2017). Bony pits in the ostrich (Struthio camelus) and emu (Dromaius novaehollandiae) bill tip. The Anatomical Record, 300, 1705-1715.
Erickson, G. M., Lappin, A. K., Parker, T., & Vliet, K. A. (2004). Comparison of bite-force performance between long-term captive and wild American alligators (Alligator mississippiensis). Journal of Zoology (London), 262, 21-28.
Evers, S. W., Joyce, W. G., Choiniere, J. N., Ferreira, G., Foth, C., Hermanson, G., Yi, H., Johnson, C. M., Werneburg, I., & Benson, R. B. J. (2022). Independent origin of large labyrinth size in turtles. Nature Communications, 13(5807), 1-15.
Evers, S. W., Ponstein, J., Jansen, M. A., Gray, J. A., & Fröbisch, J. (2022). A systematic compendium of turtle mandibular anatomy using digital dissections of soft tissue and osteology. The Anatomical Record, 306, 1-76.
Felice, R. N., & Goswami, A. (2018). Developmental origins of mosaic evolution in the avian cranium. Proceedings of the National Academy of Sciences of the United States of America, 115, 555-560.
Foley, W. J., & Kokich, V. G. (1980). The effects of mechanical immobilization on sutural development in the growing rabbit. Journal of Neurosurgery, 53, 794-801.
Foth, C., Hedrick, B. P., & Ezcurra, M. D. (2016). Cranial ontogenetic variation in early saurischians and the role of heterochrony in the diversification of predatory dinosaurs. PeerJ, 4, e1589.
Gauthier, J. A. (1986). Saurischian monophyly and the origin of birds. Memoirs of the California Academy of Sciences, 8, 1-55.
Green, T. L., & Gignac, P. M. (2020). Osteological description of casque ontogeny in the southern cassowary (Casuarius casuarius) using micro-CT imaging. Anatomical Record, 304, 461-479.
Hansford, J. P., & Turvey, S. T. (2018). Unexpected diversity within the extinct elephant birds (Aves: Aepyornithidae) and a new identity for the world's largest bird. Royal Society Open Science, 5, 1-28.
Harris, J. D. (2004). Confusing dinosaurs with mammals: Tetrapod phylogenetics and anatomical terminology in the world of homology. Anatomical Record, Part A Discoveries in Molecular, Cellular, and Evolutionary Biology, 281, 1240-1246.
Hogg, D. A. (1978). The articulations of the neurocranium in the postnatal skeleton of the domestic fowl (Gallus gallus domesticus). Journal of Anatomy, 127, 1-53.
Hu, H., Sansalone, G., Wroe, S., McDonald, P. G., O'Connor, J. K., Li, Z., Xu, X., & Zhou, Z. (2019). Evolution of the vomer and its implications for cranial kinesis in Paraves. Proceedings of the National Academy of Sciences of the United States of America, 116, 19571-19578.
Hu, H., Wang, Y., Fabbri, M., O'Connor, J. K., Mcdonald, G. P., Wroe, S., Yin, X., Zheng, X., Zhou, Z., & Benson, R. B. J. (2022). Cranial osteology and palaeobiology of the early cretaceous bird Jeholornis prima (Aves: Jeholornithiformes). Zoological Journal of the Linnean Society, 198, 93-112.
Hu, K., King, J. L., Romick, C. A., Dufeau, D. L., Witmer, L. M., Stubbs, T. L., Rayfield, E. J., & Benton, M. J. (2021). Ontogenetic endocranial shape change in alligators and ostriches and implications for the development of the non-avian dinosaur endocranium. The Anatomical Record, 304, 1759-1774.
Hutchins, H., Jackson, J. A., Bock, W. J., & Olendorf, D. (2002). Grzimek's animal life encyclopedia, birds I-IV. Gale Group.
Jollie, M. T. (1957). The head skeleton of the chicken and remarks on the anatomy of this region in other birds. Journal of Morphology, 100, 389-436.
Kawabe, S., Matsuda, S., Tsunekawa, N., & Endo, H. (2015). Ontogenetic shape change in the chicken brain: Implications for paleontology. PLoS One, 10, e0129939.
Klingenberg, C. P. (1998). Heterochrony and allometry: The analysis of evolutionary change in ontogeny. Biological Reviews, 73, 79-123.
Lautenschlager, S., Bright, J. A., & Rayfield, E. J. (2014). Digital dissection-using contrast-enhanced computed tomography scanning to elucidate hard-and soft-tissue anatomy in the common buzzard Buteo buteo. Journal of Anatomy, 224, 412-431.
Lee, H. W., Esteve-Altava, B., & Abzhanov, A. (2020). Evolutionary and ontogenetic changes of the anatomical organization and modularity in the skull of archosaurs. Scientific Reports, 10(16138), 1-13.
Livezey, B. C., & Zusi, R. L. (2006). Phylogeny of Neornithes. Bulletin of Carnegie Museum of Natural History, 37, 1-544.
Marshall, C. L. (2000). Embryonic growth patterns in ostrich and other ratite skeletons. Yale University.
Maxwell, E. E. (2008). Comparative embryonic development of the skeleton of the domestic Turkey (Meleagris gallopavo) and other galliform birds. Zoology, 2008, 242-257.
Maxwell, E. E., & Larsson, H. C. E. (2009). Comparative ossification sequence and skeletal development of the postcranium of palaeognathous birds (Aves: Palaeognathae). Zoological Journal of the Linnean Society, 157, 169-196.
Mayr, G. (2020). Comparative morphology of the avian maxillary bone (os maxillare) based on an examination of macerated juvenile skeletons. Acta Zoologica, 101, 24-38.
Mayr, G., & Manegold, A. (2020). On the comparative morphology of the juvenile avian skull: An assessment of squamosal shape across avian higher-level taxa. Anatomical Record, 304, 845-859.
Moss, M. L. (1957). Experimental alteration of sutural area morphology. The Anatomical Record, 127, 569-589.
Navalón, G., Nebreda, S. M., Bright, J. A., Fabbri, M., Benson, R. B., Bhullar, B. A., Marugán-Lobón, J., & Rayfield, E. J. (2021). Craniofacial development illuminates the evolution of nightbirds (Strisores). Proceedings of the Royal Society B, 288, 1-10.
Nice, M. M. (1962). Development of behavior in precocial birds. Transactions of the Linnaean, 8, 1-21.
O'Connor, J. K., & Chiappe, L. (2011). A revision of enantiornithine (Aves: Ornithothoraces) skull morphology. Journal of Systematic Palaeontology, 9, 135-157.
Owen, R. (1854). Descriptive catalogue of the fossil organic remains of Reptilia and Pisces contained in the Museum of the Royal College of Surgeons of England. R. & J.E. Taylor.
Parker, W. K. (1866). VIII. On the structure and development of the skull in the ostrich tribe. Philosophical Transactions of the Royal Society, 156, 113-183.
Parker, J. (1891). Observations on the anatomy and development of apteryx. Philosophical Transactions of the Royal Society of London, Series B, 182, 25-134.
Parker, W. K. (1869). XXIX. On the structure and development of the skull of the common fowl (Gallus domesticus). Philosophical Transactions of the Royal Society of London, 159, 2755-2807.
Piro, A., & Acosta Hospitaleche, C. (2019). Skull morphology and ontogenetic variation of the southern giant petrel Macronectes giganteus (Aves: Procellariiformes). Polar Biology, 42, 27-45.
Plateau, O., & Foth, C. (2020). Birds have peramorphic skulls, too: Anatomical network analyses reveal oppositional heterochronies in avian skull evolution. Communications Biology, 3(195), 1-12.
Plateau, O., & Foth, C. (2021). Common patterns of skull bone fusion and their potential to discriminate different ontogenetic stages in extant birds. Frontiers in Ecology and Evolution, 9(737199), 1-15.
Posso, S. R., & Donatelli, R. J. (2005). Skull and mandible formation in the cuckoo (Aves, Cuculidae): Contributions to the nomenclature in avian osteology and systematics. European Journal of Morphology, 42, 163-172.
Portmann, A. (1935). Die ontogenese der vögel als evolutionsproblem. Acta Biotheoretica, 1, 59-90.
Prum, R. O., Berv, J. S., Dornburg, A., Field, D. J., Townsend, J. P., Moriarty Lemmon, E., & Lemmon, A. R. (2015). A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature, 526, 569-573.
Rauhut, O. W. M. (2014). New observations on the skull of archaeopteryx. Paläontologische Zeitschrift, 88, 211-221.
Rauhut, O. W., & Foth, C. (2020). The origin of birds: Current consensus, controversy, and the occurrence of feathers. In C. Foth & O. W. Rauhut (Eds.), The evolution of feathers: From their origin to the present (pp. 27-45). Springer.
Runge, J., & Wirkner, C. S. (2019). A unified morphological scenario for the evolution of haemolymph pressure generation in spiders (Araneae: Arachnida). Zoological Journal of the Linnean Society, 186, 353-387.
Sampson, S. D., & Witmer, L. M. (2007). Craniofacial anatomy of Majungasaurus crenatissimus (Theropoda: Abelisauridae) from the late cretaceous of Madagascar. Journal of Vertebrate Paleontology, 27(sp8), 32-102.
Shibazaki, R., Dechow, P. C., Maki, K., & Opperman, L. A. (2007). Biomechanical strain and morphologic changes with age in rat calvarial bone and sutures. Plastic and Reconstructive Surgery, 119, 2167-2178.
Skutch, A. (1976). Parent birds and their young. The Corrie Herring Hooks series, No. 2. University of Texas Press.
Sosa, M. A., & Acosta Hospitaleche, C. (2018). Ontogenetic variations of the head of Aptenodytes forsteri (Aves, Sphenisciformes): Muscular and skull morphology. Polar Biology, 41, 225-235.
Sosa, M. A., & Acosta Hospitaleche, C. (2022). Postnatal ontogeny of the spine of Aptenodytes forsteri (Aves, Sphenisciformes) and modularity of the neck. Polar Biology, 45, 309-329.
Stange, M., Núñez-León, D., Sánchez-Villagra, M. R., Jensen, P., & Wilson, L. A. B. (2018). Morphological variation under domestication: How variable are chickens? Royal Society Open Science, 5(180993), 1-15.
Starck, J. M., & Ricklefs, R. E. (1998). Evolution within the altricial-precocial spectrum. In J. M. Starck & R. E. Ricklefs (Eds.), Avian growth and development (pp. 3-30). Oxford University Press.
Starck, J. M. (1993). Evolution of avian ontogenies. Current Ornithology, 10, 275-366.
Werneburg, I., Esteve-Altava, B., Bruno, J., Ladeira, M. T., & Diogo, R. (2019). Unique skull network complexity of tyrannosaurus rex among land vertebrates. Scientific Reports, 9(1520), 1-14.
Widrig, K., & Field, D. J. (2022). The evolution and fossil record of Palaeognathous birds (Neornithes: Palaeognathae). Diversity, 14, 1-105.
Wilson, J. A. (2006). Anatomical nomenclature of fossil vertebrates: Standardized terms or “lingua franca”? Journal of Vertebrate Paleontology, 26, 511-518.
Witmer, L. M., & Ridgely, R. C. (2008). The paranasal air sinuses of predatory and armored dinosaurs (Archosauria: Theropoda and Ankylosauria) and their contribution to cephalic structure. The Anatomical Record, 291, 1362-1388.
Zusi, R. L., & Livezey, B. C. (2006). Variation in the os palatinum and its structural relation to the palatum osseum of birds (Aves). Annals of Carnegie Museum, 75, 137.

Auteurs

Olivia Plateau (O)

Department of Geosciences, University of Fribourg, Fribourg, Switzerland.
Department of Earth Sciences, University of Cambridge, Cambridge, UK.

Todd L Green (TL)

Department of Anatomy, New York Institute of Technology College of Osteopathic Medicine, Old Westbury, New York, USA.

Paul M Gignac (PM)

Department of Cellular & Molecular Medicine, University of Arizona College of Medicine, Tucson, Arizona, USA.

Christian Foth (C)

Department of Geosciences, University of Fribourg, Fribourg, Switzerland.

Classifications MeSH