Insight into the evolutionary assemblage of cranial kinesis from a Cretaceous bird
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eLife assessment
Most birds today can lift the upper beak independently of the brain case, enabled by a series of mobile joints and bending zones in the skull. The computed tomography of the skull of a 120-million-year-old toothed bird produced by the authors shows for the first time that the joints were still absent, but also hints at how they may have evolved later. This compelling, important paper is of high interest to evolutionary biologists, vertebrate paleontologists (especially, but by no means only, those working on bird origins) and specialists in biomechanics.
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Abstract
The independent movements and flexibility of various parts of the skull, called cranial kinesis, are an evolutionary innovation that is found in living vertebrates only in some squamates and crown birds and is considered to be a major factor underpinning much of the enormous phenotypic and ecological diversity of living birds, the most diverse group of extant amniotes. Compared to the postcranium, our understanding of the evolutionary assemblage of the characteristic modern bird skull has been hampered by sparse fossil records of early cranial materials, with competing hypotheses regarding the evolutionary development of cranial kinesis among early members of the avialans. Here, a detailed three-dimensional reconstruction of the skull of the Early Cretaceous enantiornithine Yuanchuavis kompsosoura allows for its in-depth description, including elements that are poorly known among early-diverging avialans but are central to deciphering the mosaic assembly of features required for modern avian cranial kinesis. Our reconstruction of the skull shows evolutionary and functional conservation of the temporal and palatal regions by retaining the ancestral theropod dinosaurian configuration within the skull of this otherwise derived and volant bird. Geometric morphometric analysis of the palatine suggests that loss of the jugal process represents the first step in the structural modifications of this element leading to the kinetic crown bird condition. The mixture of plesiomorphic temporal and palatal structures together with a derived avialan rostrum and postcranial skeleton encapsulated in Yuanchuavis manifests the key role of evolutionary mosaicism and experimentation in early bird diversification.
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Author Response
Reviewer #1 (Public Review):
- Probably the shortest review I've ever written! Most birds today can lift the upper beak independently of the brain case. This is made possible by a series of mobile joints and bending zones in the skull. To investigate the evolution of this phenomenon, the authors successfully CT-scanned the thoroughly squished skull of the Early Cretaceous stem-bird Yuanchuavis. The detailed description and illustration of the shapes and positions of the skull bones leave no doubt about the conclusion that the toothed snout was unable to move independently of the brain case. They also show, however, that the loss of a few extensions from specific skull bones would have made mobility possible. This plugs a major gap in our understanding of the evolution of mobility within the skull in birds (and by …
Author Response
Reviewer #1 (Public Review):
- Probably the shortest review I've ever written! Most birds today can lift the upper beak independently of the brain case. This is made possible by a series of mobile joints and bending zones in the skull. To investigate the evolution of this phenomenon, the authors successfully CT-scanned the thoroughly squished skull of the Early Cretaceous stem-bird Yuanchuavis. The detailed description and illustration of the shapes and positions of the skull bones leave no doubt about the conclusion that the toothed snout was unable to move independently of the brain case. They also show, however, that the loss of a few extensions from specific skull bones would have made mobility possible. This plugs a major gap in our understanding of the evolution of mobility within the skull in birds (and by extension elsewhere, notably in the similarly diverse lizards & snakes).
Yes, we are delighted that this work will further advance our understandings about the avian skull evolution.
Reviewer #2 (Public Review):
- Wang et al. present a detailed description and analysis of the previously reported cranial remains of enantiornithine bird Yuanchuavis. The authors use X-ray CT scan data to reconstruct the cranial elements and retro-deform the facial and palatal skeleton. The authors also use principle component analysis with geometric morphometrics data to investigate where Yuanchuavis falls in palatine phylomorphospace. The authors use these data to make inferences about the kinetics of the Yuanchuavis skull as well as the evolution of cranial kinesis across birds. Generally, I find the authors' direct interpretation of their anatomical and PCA data to be convincing and compelling. The anatomical description is thorough and accurate. The methods used for the geometrics morphometrics and PC analyses are appropriate. I find compelling the authors' interpretations that Yuanchuavis largely retained the ancestral non-avialan akinetic skull.
One of the greatest strengths of this paper are the extremely attractive figures. In particular, I find figure 4 to be exceptionally useful - this is easily the most effective illustration I have yet seen of avian cranial kinesis and the shifts in cranial morphology that underlie its evolution. I applaud whoever designed this figure. My one major concern with this paper's methodology is that the palatine used for Ichthyornis is incorrect. Torres et al. (2021) published the correct palatines, which were very different from those incorrectly (but understandably) identified in Field et al. (2018) and used here. I strongly urge the authors to rerun their GMM analysis with corrected data
We thank the reviewer for supporting this study. As for the palatine of Ichthyornis, we have used the palatine reconstruction in Torres et al. (2021) and reperformed the GMM analyses. This certainly changes the GMM result, and the main conclusion has not been strongly influenced. We are grateful for this comment.
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eLife assessment
Most birds today can lift the upper beak independently of the brain case, enabled by a series of mobile joints and bending zones in the skull. The computed tomography of the skull of a 120-million-year-old toothed bird produced by the authors shows for the first time that the joints were still absent, but also hints at how they may have evolved later. This compelling, important paper is of high interest to evolutionary biologists, vertebrate paleontologists (especially, but by no means only, those working on bird origins) and specialists in biomechanics.
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Reviewer #1 (Public Review):
Probably the shortest review I've ever written! Most birds today can lift the upper beak independently of the brain case. This is made possible by a series of mobile joints and bending zones in the skull. To investigate the evolution of this phenomenon, the authors successfully CT-scanned the thoroughly squished skull of the Early Cretaceous stem-bird Yuanchuavis. The detailed description and illustration of the shapes and positions of the skull bones leave no doubt about the conclusion that the toothed snout was unable to move independently of the brain case. They also show, however, that the loss of a few extensions from specific skull bones would have made mobility possible. This plugs a major gap in our understanding of the evolution of mobility within the skull in birds (and by extension elsewhere, …
Reviewer #1 (Public Review):
Probably the shortest review I've ever written! Most birds today can lift the upper beak independently of the brain case. This is made possible by a series of mobile joints and bending zones in the skull. To investigate the evolution of this phenomenon, the authors successfully CT-scanned the thoroughly squished skull of the Early Cretaceous stem-bird Yuanchuavis. The detailed description and illustration of the shapes and positions of the skull bones leave no doubt about the conclusion that the toothed snout was unable to move independently of the brain case. They also show, however, that the loss of a few extensions from specific skull bones would have made mobility possible. This plugs a major gap in our understanding of the evolution of mobility within the skull in birds (and by extension elsewhere, notably in the similarly diverse lizards & snakes).
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Reviewer #2 (Public Review):
Wang et al. present a detailed description and analysis of the previously reported cranial remains of enantiornithine bird Yuanchuavis. The authors use X-ray CT scan data to reconstruct the cranial elements and retro-deform the facial and palatal skeleton. The authors also use principle component analysis with geometric morphometrics data to investigate where Yuanchuavis falls in palatine phylomorphospace. The authors use these data to make inferences about the kinetics of the Yuanchuavis skull as well as the evolution of cranial kinesis across birds.
Generally, I find the authors' direct interpretation of their anatomical and PCA data to be convincing and compelling. The anatomical description is thorough and accurate. The methods used for the geometrics morphometrics and PC analyses are appropriate. I find …
Reviewer #2 (Public Review):
Wang et al. present a detailed description and analysis of the previously reported cranial remains of enantiornithine bird Yuanchuavis. The authors use X-ray CT scan data to reconstruct the cranial elements and retro-deform the facial and palatal skeleton. The authors also use principle component analysis with geometric morphometrics data to investigate where Yuanchuavis falls in palatine phylomorphospace. The authors use these data to make inferences about the kinetics of the Yuanchuavis skull as well as the evolution of cranial kinesis across birds.
Generally, I find the authors' direct interpretation of their anatomical and PCA data to be convincing and compelling. The anatomical description is thorough and accurate. The methods used for the geometrics morphometrics and PC analyses are appropriate. I find compelling the authors' interpretations that Yuanchuavis largely retained the ancestral non-avialan akinetic skull.
One of the greatest strengths of this paper are the extremely attractive figures. In particular, I find figure 4 to be exceptionally useful - this is easily the most effective illustration I have yet seen of avian cranial kinesis and the shifts in cranial morphology that underlie its evolution. I applaud whoever designed this figure.
My one major concern with this paper's methodology is that the palatine used for Ichthyornis is incorrect. Torres et al. (2021) published the correct palatines, which were very different from those incorrectly (but understandably) identified in Field et al. (2018) and used here. I strongly urge the authors to rerun their GMM analysis with corrected data.
The remaining weaknesses I find in this paper are not major but are worth addressing, and generally pertain to the broader discussion of significance of the authors' more direct interpretations of their data. The authors' suggestion that reduction/loss of the jugal process of the palatine was an early step towards the modern kinetic avian skull is logical, but I don't think the GMM analysis presented here demonstrates that (contrary to lines 390-392). The GMM analysis can only help identify such morphological shifts, not connect them to functional shifts. Rather, I think this analysis helps refine when this shift occurred - indicating that, if there is such a functional link, the earliest steps towards the modern kinetic skull occurred early in avialan evolution.
I find the discussion of the evolution of cranial kinesis as exaptation (lines 427-441) confusing, distracting and largely unnecessary. Has anyone previously suggested that avian cranial kinesis is an example of preadaptation?
I am similarly confused by the connection made by the authors of evolutionary modularity, the akinetic skull of enantiornithines and patterns of avialan diversification (lines 442-464). Specifically, I do not understand how the dominance of enantiornithine clade in the Cretaceous is "counterintuitive" (line 452), nor do I understand how this pattern is explained by evolutionary modularity.
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