Bone tissue histology of the Early Cretaceous bird<i>Yanornis</i>: evidence for a diphyletic origin of modern avian growth strategies within Ornithuromorpha

Wang, Junyou; Hao, Xiuzhi; Kundrát, Martin; Liu, Zhiping; Uesugi, Kentaro; Jurasekova, Z.; Guo, Bin; Hoshino, Masato; Li, Yaoquan; Monfroy, Quentin T.; Zhou, Bin; Fabriciová, Gabriela; Kang, Ai; Wang, Mei; Si, Yunhui; Gao, Jie; Xu, Guangqiong; Li, Zhen

doi:10.1080/08912963.2019.1593405

Cited by 19 publications

(49 citation statements)

References 38 publications

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“…2; O’Connor et al, 2015) suggests that the growth strategy observed in extant birds evolved independently in the Early Cretaceous outside the Ornithurae (O’Connor et al, 2015) but still in the crownward lineage that includes all extant birds. Similar results were also found in the non-ornithurine ornithuromorph Yanornis (Wang et al, 2019). Several studies also indicate that most stem birds, like their non-avian dinosaurian relatives, achieved reproductive maturity prior to skeletal maturity (O’Connor et al, 2014, 2018).…”

Section: The “Growth Age” Of Dinosaur Histologysupporting

confidence: 83%

Dinosaur paleohistology: review, trends and new avenues of investigation

Bailleul

O’Connor

Schweitzer

2019

PeerJ

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In the mid-19th century, the discovery that bone microstructure in fossils could be preserved with fidelity provided a new avenue for understanding the evolution, function, and physiology of long extinct organisms. This resulted in the establishment of paleohistology as a subdiscipline of vertebrate paleontology, which has contributed greatly to our current understanding of dinosaurs as living organisms. Dinosaurs are part of a larger group of reptiles, the Archosauria, of which there are only two surviving lineages, crocodilians and birds. The goal of this review is to document progress in the field of archosaur paleohistology, focusing in particular on the Dinosauria. We briefly review the “growth age” of dinosaur histology, which has encompassed new and varied directions since its emergence in the 1950s, resulting in a shift in the scientific perception of non-avian dinosaurs from “sluggish” reptiles to fast-growing animals with relatively high metabolic rates. However, fundamental changes in growth occurred within the sister clade Aves, and we discuss this major evolutionary transition as elucidated by histology. We then review recent innovations in the field, demonstrating how paleohistology has changed and expanded to address a diversity of non-growth related questions. For example, dinosaur skull histology has elucidated the formation of curious cranial tissues (e.g., “metaplastic” tissues), and helped to clarify the evolution and function of oral adaptations, such as the dental batteries of duck-billed dinosaurs. Lastly, we discuss the development of novel techniques with which to investigate not only the skeletal tissues of dinosaurs, but also less-studied soft-tissues, through molecular paleontology and paleohistochemistry—recently developed branches of paleohistology—and the future potential of these methods to further explore fossilized tissues. We suggest that the combination of histological and molecular methods holds great potential for examining the preserved tissues of dinosaurs, basal birds, and their extant relatives. This review demonstrates the importance of traditional bone paleohistology, but also highlights the need for innovation and new analytical directions to improve and broaden the utility of paleohistology, in the pursuit of more diverse, highly specific, and sensitive methods with which to further investigate important paleontological questions.

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Section: The “Growth Age” Of Dinosaur Histologysupporting

confidence: 83%

Dinosaur paleohistology: review, trends and new avenues of investigation

Bailleul

O’Connor

Schweitzer

2019

PeerJ

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“…Oppositional heterochronies can be further found in the growth evolution of birds, in which the somatic growth of crown birds is characterized by a short duration, but high speed 14,15 . When compared with the mode of their ancestors 38,39 , the former growth pattern represents a progenetic paedomorphosis, while the latter is an accelerated peramorphosis 40,41 . Finally, oppositional heterochronies have been further suggested for arthropod heads 42 and human skull evolution 43 .…”

Section: Juvenile Birdsmentioning

confidence: 99%

Birds have peramorphic skulls, too: anatomical network analyses reveal oppositional heterochronies in avian skull evolution

Plateau

Foth

2020

Commun Biol

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In contrast to the vast majority of reptiles, the skulls of adult crown birds are characterized by a high degree of integration due to bone fusion, e.g., an ontogenetic event generating a net reduction in the number of bones. To understand this process in an evolutionary context, we investigate postnatal ontogenetic changes in the skulls of crown bird and non-avian theropods using anatomical network analysis (AnNA). Due to the greater number of bones and bone contacts, early juvenile crown birds have less integrated skulls, resembling their nonavian theropod ancestors, including Archaeopteryx lithographica and Ichthyornis dispars. Phylogenetic comparisons indicate that skull bone fusion and the resulting modular integration represent a peramorphosis (developmental exaggeration of the ancestral adult trait) that evolved late during avialan evolution, at the origin of crown-birds. Succeeding the general paedomorphic shape trend, the occurrence of an additional peramorphosis reflects the mosaic complexity of the avian skull evolution.

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“…fully terrestrial runners, hind limb divers, aquaflyers, soarers, active flyers) and typically reaching full somatic maturity in less than a year (Brusatte et al., 2015; Habib & Ruff, 2008; Prondvai et al., 2020). Since the description of Archaeopteryx by Richard Owen in 1863, birds have been the object of numerous integrative comparative anatomical, physiological and ecological studies over the past 20 years, as fossils from all the major groups of basal avians have been excavated and described, prominently from the Early Cretaceous of China (Chinsamy et al., 2020; Wang, Hao, et al., 2019; Wang, Cau, et al., 2020; Wang, Huang, et al., 2020). When it comes to the descriptions and analysis of the microstructure in long bones, the majority of histological studies were performed using physical sections in the midshaft of the same single bone from one or several individuals from the same species, mainly due to the rarity and/or the state of preservation of the analysed species (Bailleul et al., 2019; Bell et al., 2010; Chinsamy, 2002; Gao et al., 2012; Wang et al., 2014; Wang, Huang, et al., 2020).…”

Section: Introductionmentioning

confidence: 99%

The osteohistological variability in the evolution of basal avialans

Monfroy

Kundrát

2021

Acta Zoologica

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Basal avialans have been the focus of numerous histological studies in the past decade, from which different osteohistological patterns have been described. In this review, we look at the osteohistology in selected specimens from the four major avian groups: the long‐tailed Avialae (Archaeopteryx and Jeholornithiformes), basal Pygostylia, Enantiornithes and Euornithes. Developmental and evolutionary changes in the three major bone layers are observed throughout the bone cortex of the limbs, may it be interspecific or intraspecific. Most noteworthy is the adaptive change from the overall lamellar/parallel‐fibered bone tissue to a fibrolamellar complex in the mid‐cortex as of the basal Pygostylia, potentially even as of the Jeholornithiformes. This change is generally associated with an increase in the density and complexity of the neurovascular network. Another evolutionary‐developmental feature is the progressive loss of post‐natal growth marks as of the non‐ornithurine Euornithes, indicative of uninterrupted bone growth as observed in extant Neornithes. Our comparisons of the osteohistological patterns allow us to better determine how and when specific features typical observed in the avian crown group developed, associated with external and internal factors, and how they lead to what is commonly observed in extant Neornithes.

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Bone tissue histology of the Early Cretaceous birdYanornis: evidence for a diphyletic origin of modern avian growth strategies within Ornithuromorpha

Cited by 19 publications

References 38 publications

Dinosaur paleohistology: review, trends and new avenues of investigation

Dinosaur paleohistology: review, trends and new avenues of investigation

Birds have peramorphic skulls, too: anatomical network analyses reveal oppositional heterochronies in avian skull evolution

The osteohistological variability in the evolution of basal avialans

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