Novel neuroanatomical integration and scaling define avian brain shape evolution and development
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Evaluation Summary:
Watanabe and colleagues analyse endocasts from extant (and some fossil) material to identify the distinct evolutionary and developmental patterns governing the growth and scaling relationships found in avian brains. The use of sophisticated geometric morphometrics, high-quality digital endocasts, and a suite of multivariate statistical tests robustly support the findings asserted in the paper, namely that crown birds exhibit a distinct allometric relationship that dictates their brain evolution and development. This paper is of broad interest to those working in comparative and evolutionary neuroanatomy as well as vertebrate paleontology.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1, Reviewer #2 and Reviewer #3 agreed to share their names with the authors.)
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Abstract
How do large and unique brains evolve? Historically, comparative neuroanatomical studies have attributed the evolutionary genesis of highly encephalized brains to deviations along, as well as from, conserved scaling relationships among brain regions. However, the relative contributions of these concerted (integrated) and mosaic (modular) processes as drivers of brain evolution remain unclear, especially in non-mammalian groups. While proportional brain sizes have been the predominant metric used to characterize brain morphology to date, we perform a high-density geometric morphometric analysis on the encephalized brains of crown birds (Neornithes or Aves) compared to their stem taxa—the non-avialan coelurosaurian dinosaurs and Archaeopteryx . When analyzed together with developmental neuroanatomical data of model archosaurs ( Gallus , Alligator ), crown birds exhibit a distinct allometric relationship that dictates their brain evolution and development. Furthermore, analyses by neuroanatomical regions reveal that the acquisition of this derived shape-to-size scaling relationship occurred in a mosaic pattern, where the avian-grade optic lobe and cerebellum evolved first among non-avialan dinosaurs, followed by major changes to the evolutionary and developmental dynamics of cerebrum shape after the origin of Avialae. Notably, the brain of crown birds is a more integrated structure than non-avialan archosaurs, implying that diversification of brain morphologies within Neornithes proceeded in a more coordinated manner, perhaps due to spatial constraints and abbreviated growth period. Collectively, these patterns demonstrate a plurality in evolutionary processes that generate encephalized brains in archosaurs and across vertebrates.
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Evaluation Summary:
Watanabe and colleagues analyse endocasts from extant (and some fossil) material to identify the distinct evolutionary and developmental patterns governing the growth and scaling relationships found in avian brains. The use of sophisticated geometric morphometrics, high-quality digital endocasts, and a suite of multivariate statistical tests robustly support the findings asserted in the paper, namely that crown birds exhibit a distinct allometric relationship that dictates their brain evolution and development. This paper is of broad interest to those working in comparative and evolutionary neuroanatomy as well as vertebrate paleontology.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. …
Evaluation Summary:
Watanabe and colleagues analyse endocasts from extant (and some fossil) material to identify the distinct evolutionary and developmental patterns governing the growth and scaling relationships found in avian brains. The use of sophisticated geometric morphometrics, high-quality digital endocasts, and a suite of multivariate statistical tests robustly support the findings asserted in the paper, namely that crown birds exhibit a distinct allometric relationship that dictates their brain evolution and development. This paper is of broad interest to those working in comparative and evolutionary neuroanatomy as well as vertebrate paleontology.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1, Reviewer #2 and Reviewer #3 agreed to share their names with the authors.)
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Reviewer #3 (Public Review):
The research presented by Watanabe et al. "Novel neuroanatomical integration and scaling define avian brain shape evolution and development" try to present a novel overview about how the avian brain develops and evolved. In this attemp the authors explains perfectly how integration/mopdularity worked in shaping the avian brain.
The data and analyses performed and sound, and the conclusions are well fundamented. The discussion section is extremelly atractive. The main strenghts of this research are the analyses (various analyses) performed with sound data. All the methodology is well described and easy to follow (altough I one of those persons who is not that friendly with R) so I think it will be good to have all the scripts used published together with the manuscript). Discussion and conclusions are well …
Reviewer #3 (Public Review):
The research presented by Watanabe et al. "Novel neuroanatomical integration and scaling define avian brain shape evolution and development" try to present a novel overview about how the avian brain develops and evolved. In this attemp the authors explains perfectly how integration/mopdularity worked in shaping the avian brain.
The data and analyses performed and sound, and the conclusions are well fundamented. The discussion section is extremelly atractive. The main strenghts of this research are the analyses (various analyses) performed with sound data. All the methodology is well described and easy to follow (altough I one of those persons who is not that friendly with R) so I think it will be good to have all the scripts used published together with the manuscript). Discussion and conclusions are well justified and excellently presented. Graphics are wonderful and self-explanatory.
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Reviewer #2 (Public Review):
Watanabe et al. investigated avian brain evolution and development via morphometric analysis of endocast size, shape, and modularity. They incorporate developmental data from extant archosaurs (Gallus and Alligator) with endocasts of crown birds and non-avialan coelurosaurian dinosaurs to identify the allometric relationship and evolution of highly encephalised crown bird brains.
Major strengths of the methods include the sophisticated geometric morphometric approach with digital endocast data to characterise variation in both overall brain morphology, and that of its various functional subdivisions. The authors further attempt to quantify the relative contributions of the integrated vs. modular processes between major brain regions. Further parallels with mammals, another group to have achieved highly …
Reviewer #2 (Public Review):
Watanabe et al. investigated avian brain evolution and development via morphometric analysis of endocast size, shape, and modularity. They incorporate developmental data from extant archosaurs (Gallus and Alligator) with endocasts of crown birds and non-avialan coelurosaurian dinosaurs to identify the allometric relationship and evolution of highly encephalised crown bird brains.
Major strengths of the methods include the sophisticated geometric morphometric approach with digital endocast data to characterise variation in both overall brain morphology, and that of its various functional subdivisions. The authors further attempt to quantify the relative contributions of the integrated vs. modular processes between major brain regions. Further parallels with mammals, another group to have achieved highly encephalised brains, could expand the appeal of this paper to a broader audience.
The major findings of the paper, that crown birds possess a distinct brain shape-to-size scaling relationship with a more integrated brain structure compared to non-avialan archosaurs, are supported. Aside from those working on archosaurian brain evolution, this paper provides a valuable example in advanced methodology and approach to studying neural evolution more broadly.
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Reviewer #1 (Public Review):
Watanabe and colleagues investigated how properties intrinsic to the organism (allometry, development, morphological integration) have directed the evolution of encephalized and diverse brains in avian and non-avian dinosaurs, on the basis of 3-D imaging, high-density shape data of endocasts from 37 extant and recently extinct crown bird species, 6 non-avian coelurosaurian dinosaurs, and Archaeopteryx, as well as developmental neuroanatomical data of model archosaurs (Gallus, Alligator). Using the methods for multivariate analysis and for evaluating the pattern of integration, they demonstrate that extant birds have a distinct allometric, more integrated brain structure than non-avian dinosaurs closely related to birds. This study reveals complexity in evolutionary processes (concerted and/or mosaic …
Reviewer #1 (Public Review):
Watanabe and colleagues investigated how properties intrinsic to the organism (allometry, development, morphological integration) have directed the evolution of encephalized and diverse brains in avian and non-avian dinosaurs, on the basis of 3-D imaging, high-density shape data of endocasts from 37 extant and recently extinct crown bird species, 6 non-avian coelurosaurian dinosaurs, and Archaeopteryx, as well as developmental neuroanatomical data of model archosaurs (Gallus, Alligator). Using the methods for multivariate analysis and for evaluating the pattern of integration, they demonstrate that extant birds have a distinct allometric, more integrated brain structure than non-avian dinosaurs closely related to birds. This study reveals complexity in evolutionary processes (concerted and/or mosaic patterns) that shape the evolution of encephalized and divergent brains across vertebrates, birds in particular.
The inference in the manuscript is overall clear, and the conclusions are well supported by data, which in turn will be informative for relevant or follow-up studies. Due to the paucity of the endocast data from early birds, some claims sourced from the present data could be proposed more cautiously (e.g. in the abstract), like the way on page 10.
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