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Title: A diminutive perinate European Enantiornithes reveals an asynchronous ossification pattern in early birds

Abstract

Fossils of juvenile Mesozoic birds provide insight into the early evolution of avian development, however such fossils are rare. The analysis of the ossification sequence in these early-branching birds has the potential to address important questions about their comparative developmental biology and to help understand their morphological evolution and ecological differentiation. Here we report on an early juvenile enantiornithine specimen from the Early Cretaceous of Europe, which sheds new light on the osteogenesis in this most species-rich clade of Mesozoic birds. Consisting of a nearly complete skeleton, it is amongst the smallest known Mesozoic avian fossils representing post-hatching stages of development. Finally, comparisons between this new specimen and other known early juvenile enantiornithines support a clade-wide asynchronous pattern of osteogenesis in the sternum and the vertebral column, and strongly indicate that the hatchlings of these phylogenetically basal birds varied greatly in size and tempo of skeletal maturation.

Authors:
ORCiD logo [1];  [2]; ORCiD logo [3]; ORCiD logo [4];  [5];  [6]; ORCiD logo [6];  [7]; ORCiD logo [8]; ORCiD logo [9];  [10]; ORCiD logo [11]; ORCiD logo [8]; ORCiD logo [11]
+ Show Author Affiliations
  1. ARAID—Fundacion Conjunto Paleontologico de Teruel-Dinopolis, Teruel (Spain); Univ. of Manchester (United Kingdom). School of Earth and Environmental Sciences
  2. Natural History Museum of Los Angeles County, Los Angeles, CA (United States). Dinosaur Inst.
  3. Uppsala Univ. (Sweden). Dept. of Organismal Biology; European Synchrotron Radiation Facility (ESRF), Grenoble (France)
  4. Univ. of Manchester (United Kingdom). School of Earth and Environmental Sciences; Natural History Museum, London (United Kingdom). Dept. of Earth Sciences
  5. Univ. of Manchester (United Kingdom). School of Earth and Environmental Sciences; SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
  6. Univ. of Manchester (United Kingdom). School of Earth and Environmental Sciences
  7. Univ. of Manchester (United Kingdom). School of Earth and Environmental Sciences; College of Charleston, Charleston, SC (United States). Dept. of Geology and Environmental Geosciences
  8. Univ. Nacional de Educacion a Distancia, Madrid (Spain)
  9. Natural History Museum of Los Angeles County, Los Angeles, CA (United States). Dinosaur Inst.; Univ. de Malaga, Malaga (Spain)
  10. Natural History Museum of Los Angeles County, Los Angeles, CA (United States). Dinosaur Inst.; Univ. Autonoma de Madrid (Spain). Facultad de Ciencias
  11. Univ. Autonoma de Madrid (Spain). Facultad de Ciencias
Publication Date:
Research Org.:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Sponsoring Org.:
USDOE; European Union (EU)
OSTI Identifier:
1437354
Grant/Contract Number:  
AC02-76SF00515
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Knoll, Fabien, Chiappe, Luis M., Sanchez, Sophie, Garwood, Russell J., Edwards, Nicholas P., Wogelius, Roy A., Sellers, William I., Manning, Phillip L., Ortega, Francisco, Serrano, Francisco J., Marugan-Lobon, Jesus, Cuesta, Elena, Escaso, Fernando, and Sanz, Jose Luis. A diminutive perinate European Enantiornithes reveals an asynchronous ossification pattern in early birds. United States: N. p., 2018. Web. doi:10.1038/s41467-018-03295-9.
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Knoll, Fabien, Chiappe, Luis M., Sanchez, Sophie, Garwood, Russell J., Edwards, Nicholas P., Wogelius, Roy A., Sellers, William I., Manning, Phillip L., Ortega, Francisco, Serrano, Francisco J., Marugan-Lobon, Jesus, Cuesta, Elena, Escaso, Fernando, & Sanz, Jose Luis. A diminutive perinate European Enantiornithes reveals an asynchronous ossification pattern in early birds. United States. https://doi.org/10.1038/s41467-018-03295-9
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Knoll, Fabien, Chiappe, Luis M., Sanchez, Sophie, Garwood, Russell J., Edwards, Nicholas P., Wogelius, Roy A., Sellers, William I., Manning, Phillip L., Ortega, Francisco, Serrano, Francisco J., Marugan-Lobon, Jesus, Cuesta, Elena, Escaso, Fernando, and Sanz, Jose Luis. Mon . "A diminutive perinate European Enantiornithes reveals an asynchronous ossification pattern in early birds". United States. https://doi.org/10.1038/s41467-018-03295-9. https://www.osti.gov/servlets/purl/1437354.
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@article{osti_1437354,
title = {A diminutive perinate European Enantiornithes reveals an asynchronous ossification pattern in early birds},
author = {Knoll, Fabien and Chiappe, Luis M. and Sanchez, Sophie and Garwood, Russell J. and Edwards, Nicholas P. and Wogelius, Roy A. and Sellers, William I. and Manning, Phillip L. and Ortega, Francisco and Serrano, Francisco J. and Marugan-Lobon, Jesus and Cuesta, Elena and Escaso, Fernando and Sanz, Jose Luis},
abstractNote = {Fossils of juvenile Mesozoic birds provide insight into the early evolution of avian development, however such fossils are rare. The analysis of the ossification sequence in these early-branching birds has the potential to address important questions about their comparative developmental biology and to help understand their morphological evolution and ecological differentiation. Here we report on an early juvenile enantiornithine specimen from the Early Cretaceous of Europe, which sheds new light on the osteogenesis in this most species-rich clade of Mesozoic birds. Consisting of a nearly complete skeleton, it is amongst the smallest known Mesozoic avian fossils representing post-hatching stages of development. Finally, comparisons between this new specimen and other known early juvenile enantiornithines support a clade-wide asynchronous pattern of osteogenesis in the sternum and the vertebral column, and strongly indicate that the hatchlings of these phylogenetically basal birds varied greatly in size and tempo of skeletal maturation.},
doi = {10.1038/s41467-018-03295-9},
journal = {Nature Communications},
number = 1,
volume = 9,
place = {United States},
year = {Mon Mar 05 00:00:00 EST 2018},
month = {Mon Mar 05 00:00:00 EST 2018}
}
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Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1038/s41467-018-03295-9
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Citation Metrics:
Cited by: 27 works
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Figures / Tables:

Fig. 1 Fig. 1: Overview photographs of the slab and counterslab of MPCM-LH-26189. Slab a is on the left, slab b, on the right. The two red boxes indicate the localisation of the areas analysed histologically (Fig. 3). Abbreviations: An: angular, Ar: articular, CaV: caudal vertebrae, CeV: cervical vertebrae, Co: coracoid, De:more » dentary, DoV: dorsal vertebrae, Fe: femur, Fr: frontal, Ga: gastralium, Hu: humerus, Hy: hyoid, Is: ischium, Ju: jugal, MiMC: minor metacarpal, Pu: pubis, Qu: quadrate, Ra: radius, Ri: rib, Sa: surangular, Sp: splenial, SaV: sacral vertebrae, SR: sclerotic ring, St: sternum, Ti: tibia, Ul: ulna« less
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Works referenced in this record:

Insights into the evolution of rachis dominated tail feathers from a new basal enantiornithine (Aves: Ornithothoraces)
journal, October 2014

  • Wang, Xiaoli; O'Connor, Jingmai K.; Zheng, Xiaoting
  • Biological Journal of the Linnean Society, Vol. 113, Issue 3
  • DOI: 10.1111/bij.12313

First species of Enantiornithes from Sihedang elucidates skeletal development in Early Cretaceous enantiornithines
journal, November 2016

A revision of enantiornithine (Aves: Ornithothoraces) skull morphology
journal, February 2011

Timing of Ossification in Duck, Quail, and Zebra Finch: lntraspecific Variation, Heterochronies, and Life History Evolution
journal, July 2011

  • Mitgutsch, Christian; Wimmer, Corinne; Sánchez-Villagra, Marcelo R.
  • Zoological Science, Vol. 28, Issue 7
  • DOI: 10.2108/zsj.28.491

Vertebral architecture in the earliest stem tetrapods
journal, January 2013

  • Pierce, Stephanie E.; Ahlberg, Per E.; Hutchinson, John R.
  • Nature, Vol. 494, Issue 7436
  • DOI: 10.1038/nature11825

An Early Cretaceous pellet
journal, February 2001

  • Sanz, José L.; Chiappe, Luis M.; Fernádez-Jalvo, Yolanda
  • Nature, Vol. 409, Issue 6823
  • DOI: 10.1038/35059172

Insight into the growth pattern and bone fusion of basal birds from an Early Cretaceous enantiornithine bird
journal, October 2017

  • Wang, Min; Li, Zhiheng; Zhou, Zhonghe
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 43
  • DOI: 10.1073/pnas.1707237114

A reappraisal of Cerebavis cenomanica (Aves, Ornithurae), from Melovatka, Russia
journal, November 2015

  • Walsh, Stig A.; Milner, Angela C.; Bourdon, Estelle
  • Journal of Anatomy, Vol. 229, Issue 2
  • DOI: 10.1111/joa.12406

Ossification sequence of the avian order anseriformes, with comparison to other precocial birds
journal, September 2008

Three-Dimensional Synchrotron Virtual Paleohistology: A New Insight into the World of Fossil Bone Microstructures
journal, October 2012

  • Sanchez, Sophie; Ahlberg, Per E.; Trinajstic, Katherine M.
  • Microscopy and Microanalysis, Vol. 18, Issue 5
  • DOI: 10.1017/S1431927612001079

Evolution of growth pattern in birds
journal, July 2001

  • Chinsamy, Anusuya; Elzanowski, Andrzej
  • Nature, Vol. 412, Issue 6845
  • DOI: 10.1038/35086650

A Precocial Avian Embryo from the Lower Cretaceous of China
journal, October 2004

Skeletal Development at the Time of Fledging in House Wrens
journal, August 1998

  • Dutta, Chaitali; Johnson, L. Scott; Larkin, David
  • The Condor, Vol. 100, Issue 3
  • DOI: 10.2307/1369728

Deep-time evolution of regeneration and preaxial polarity in tetrapod limb development
journal, October 2015

  • Fröbisch, Nadia B.; Bickelmann, Constanze; Olori, Jennifer C.
  • Nature, Vol. 527, Issue 7577
  • DOI: 10.1038/nature15397

A Primitive Enantiornithine Bird and the Origin of Feathers
journal, December 2000

Evolution and functional significance of derived sternal ossification patterns in ornithothoracine birds
journal, July 2015

  • O'Connor, J. K.; Zheng, X. -T.; Sullivan, C.
  • Journal of Evolutionary Biology, Vol. 28, Issue 8
  • DOI: 10.1111/jeb.12675

An Early Cretaceous bird from Spain and its implications for the evolution of avian flight
journal, August 1996

  • Sanz, José L.; Chiappe, Luis M.; Pérez-Moreno, Bernardino P.
  • Nature, Vol. 382, Issue 6590
  • DOI: 10.1038/382442a0

Juvenile Birds from the Early Cretaceous of China: Implications for Enantiornithine Ontogeny
journal, January 2007

Multivariate analysis of neognath skeletal measurements: implications for body mass estimation in Mesozoic birds: Body Mass Estimation in Stem Birds
journal, February 2015

  • Serrano, Francisco José; Palmqvist, Paul; Sanz, José Luis
  • Zoological Journal of the Linnean Society, Vol. 173, Issue 4
  • DOI: 10.1111/zoj.12215

Histological observations of Enantiornithine bone (Saurischia, Aves) from the Lower Cretaceous of Las Hoyas (Spain)
journal, July 2006

  • Cambra-Moo, Oscar; Buscalioni, Ángela Delgado; Cubo, Jorge
  • Comptes Rendus Palevol, Vol. 5, Issue 5
  • DOI: 10.1016/j.crpv.2005.12.018

Mummified precocial bird wings in mid-Cretaceous Burmese amber
journal, June 2016

  • Xing, Lida; McKellar, Ryan C.; Wang, Min
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms12089

A large bird from the Early Cretaceous of China: new information on the skull of enantiornithines
journal, September 2013

Reidentification of Avian Embryonic Remains from the Cretaceous of Mongolia
journal, June 2015

Evolutionary origins of the avian brain
journal, July 2013

  • Balanoff, Amy M.; Bever, Gabe S.; Rowe, Timothy B.
  • Nature, Vol. 501, Issue 7465
  • DOI: 10.1038/nature12424

An embryonic enantiornithine bird and associated eggs from the cretaceous of Mongolia
journal, December 2013

  • Kurochkin, E. N.; Chatterjee, S.; Mikhailov, K. E.
  • Paleontological Journal, Vol. 47, Issue 11
  • DOI: 10.1134/S0031030113110087

The first enantiornithine bird from the Upper Cretaceous of China
journal, January 2014

Mesozoic avian bone microstructure: physiological implications
journal, January 1995

Bone surface texture as an ontogenetic indicator in long bones of the Canada goose Branta canadensis (Anseriformes: Anatidae)
journal, October 2006

  • Tumarkin-Deratzian, Allison R.; Vann, David R.; Dodson, Peter
  • Zoological Journal of the Linnean Society, Vol. 148, Issue 2
  • DOI: 10.1111/j.1096-3642.2006.00232.x

Growth rings in Mesozoic birds
journal, March 1994

  • Chinsamy, Anusuya; Chiappe, Luis M.; Dodson, Peter
  • Nature, Vol. 368, Issue 6468
  • DOI: 10.1038/368196a0

A New Juvenile Specimen of Sapeornis (Pygostylia: Aves) from the Lower Cretaceous of Northeast China and Allometric Scaling of this Basal Bird
journal, April 2013

Soft-tissue and dermal arrangement in the wing of an Early Cretaceous bird: Implications for the evolution of avian flight
journal, October 2015

  • Navalón, Guillermo; Marugán-Lobón, Jesús; Chiappe, Luis M.
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep14864

Anatomy of the Early Cretaceous Enantiornithine Bird Rapaxavis pani
journal, September 2011

  • O'Connor, Jingmai K.; Chiappe, Luis M.; Gao, Chunling
  • Acta Palaeontologica Polonica, Vol. 56, Issue 3
  • DOI: 10.4202/app.2010.0047

Insight into the early evolution of the avian sternum from juvenile enantiornithines
journal, January 2012

  • Zheng, Xiaoting; Wang, Xiaoli; O'Connor, Jingmai
  • Nature Communications, Vol. 3, Issue 1
  • DOI: 10.1038/ncomms2104

A bizarre Early Cretaceous enantiornithine bird with unique crural feathers and an ornithuromorph plough-shaped pygostyle
journal, January 2017

  • Wang, Min; O’Connor, Jingmai K.; Pan, Yanhong
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/ncomms14141

A Mesozoic bird from Gondwana preserving feathers
journal, June 2015

  • de Souza Carvalho, Ismar; Novas, Fernando E.; Agnolín, Federico L.
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms8141

Timing of ossification in duck, quail, and zebra finch: intraspecific variation, heterochronies, and life history evolution
text, January 2011

  • Mitgutsch, C.; Wimmer, C.; Sánchez-Villagra, M. R.
  • Zoological Society of Japan
  • DOI: 10.5167/uzh-48739

The first enantiornithine bird from the Upper Cretaceous of China
dataset, January 2014

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    Works referencing / citing this record:

    Osteohistology and Life History of the Basal Pygostylian, Confuciusornis sanctus
    journal, November 2019

    • Chinsamy, Anusuya; Marugán‐Lobón, Jesús; Serrano, Francisco J.
    • The Anatomical Record, Vol. 303, Issue 4
    • DOI: 10.1002/ar.24282

    Avian tail ontogeny, pygostyle formation, and interpretation of juvenile Mesozoic specimens
    journal, June 2018

    A fully feathered enantiornithine foot and wing fragment preserved in mid-Cretaceous Burmese amber
    journal, January 2019

    Fully fledged enantiornithine hatchling revealed by Laser-Stimulated Fluorescence supports precocial nesting behavior
    journal, March 2019

    An unusual bird (Theropoda, Avialae) from the Early Cretaceous of Japan suggests complex evolutionary history of basal birds
    journal, November 2019

    Avian palaeoneurology: Reflections on the eve of its 200th anniversary
    journal, January 2020

    • Knoll, Fabien; Kawabe, Soichiro
    • Journal of Anatomy, Vol. 236, Issue 6
    • DOI: 10.1111/joa.13160

    Dinosaur paleohistology: review, trends and new avenues of investigation
    journal, January 2019

    • Bailleul, Alida M.; O’Connor, Jingmai; Schweitzer, Mary H.
    • PeerJ, Vol. 7
    • DOI: 10.7717/peerj.7764
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