Coronary artery established through amniote evolution
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Mizukami et al. propose a scenario for the evolutionary origin of the coronary artery in amniotes by comparing the morphologies of the vasculatures across several species and developmental timepoints. They show that the coronary arteries of non-amniotes most closely resemble embryonic amniote aortic subepicardial vessels (ASVs), which are replaced by the true coronary arteries during amniote development. While the identification of common vascular structures in diverse taxa is a valuable contribution, additional developmental evidence is needed to confirm that such vessels are truly homologous.
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Abstract
Coronary arteries are a critical part of the vascular system and provide nourishment to the heart. In humans, even minor defects in coronary arteries can be lethal, emphasizing their importance for survival. However, some teleosts survive without coronary arteries, suggesting that there may have been some evolutionary changes in the morphology and function of coronary arteries in the tetrapod lineage. Here, we propose that the true ventricular coronary arteries were newly established during amniote evolution through remodeling of the ancestral coronary vasculature. In mouse ( Mus musculus ) and Japanese quail ( Coturnix japonica ) embryos, the coronary arteries unique to amniotes are established by the reconstitution of transient vascular plexuses: aortic subepicardial vessels (ASVs) in the outflow tract and the primitive coronary plexus on the ventricle. In contrast, amphibians ( Hyla japonica , Lithobates catesbeianus , Xenopus laevis , and Cynops pyrrhogaster ) retain the ASV-like vasculature as truncal coronary arteries throughout their lives and have no primitive coronary plexus. The anatomy and development of zebrafish ( Danio rerio ) and chondrichthyans suggest that their hypobranchial arteries are ASV-like structures serving as the root of the coronary vasculature throughout their lives. Thus, the ventricular coronary artery of adult amniotes is a novel structure that has acquired a new remodeling process, while the ASVs, which occur transiently during embryonic development, are remnants of the ancestral coronary vessels. This evolutionary change may be related to the modification of branchial arteries, indicating considerable morphological changes underlying the physiological transition during amniote evolution.
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Author Response
eLife assessment
Mizukami et al. propose a scenario for the evolutionary origin of the coronary artery in amniotes by comparing the morphologies of the vasculatures across several species and developmental timepoints. They show that the coronary arteries of non-amniotes most closely resemble embryonic amniote aortic subepicardial vessels (ASVs), which are replaced by the true coronary arteries during amniote development. While the identification of common vascular structures in diverse taxa is a valuable contribution, additional developmental evidence is needed to confirm that such vessels are truly homologous.
We have extensively revised our paper by including additional animal data and references. While we were unable to obtain useful data on lungfish or coelacanth, we have obtained new data related to the …
Author Response
eLife assessment
Mizukami et al. propose a scenario for the evolutionary origin of the coronary artery in amniotes by comparing the morphologies of the vasculatures across several species and developmental timepoints. They show that the coronary arteries of non-amniotes most closely resemble embryonic amniote aortic subepicardial vessels (ASVs), which are replaced by the true coronary arteries during amniote development. While the identification of common vascular structures in diverse taxa is a valuable contribution, additional developmental evidence is needed to confirm that such vessels are truly homologous.
We have extensively revised our paper by including additional animal data and references. While we were unable to obtain useful data on lungfish or coelacanth, we have obtained new data related to the physiology of coronary artery, which has been added to Fig. 7. We have also attempted to compare blood vessels at the molecular level, but found that gene expression patterns in blood vessels throughout the body were not always conserved between lineages, making it difficult to make comparisons between amphibians and amniotes. However, based on comparative morphological analysis using newly added three-dimensional data, it is reasonable to consider the amniotes' ASVs and amphibians' ASV-like vessels to be homologous.
Reviewer #3 (Public Review):
Mizukami et al. compare the structure of the coronary arteries in multiple species of amniotes, amphibians, and fish. By selecting species from each of these taxa, the authors were able to evaluate modifications to the coronary arteries during key evolutionary transitions. In mice and quail, they show two populations of vessels that are visible on the developing heart-true coronary arteries on the ventricle and a second population of vessels on the outflow tract known as the ASV., They found that in amphibians, outflow tract vessels were present but ventricular coronary arteries were completely absent. In zebrafish (a more ancestral species) an arterial branch off the rostral section of the hypobranchial artery was shown to have similar anatomical features to outflow tract vessels found in higher organisms. These zebrafish outflow tract arteries also appeared conserved in several chondriichthyes specimens. The authors conclude that rearrangement of the outflow tract vasculature or hypobranchial arteries in fish during evolution, could be homologous to the ASV population of coronary arteries in amphibians and amniotes. These data give new insight into the evolutionary origins of the coronary vasculature.
Major Points
- The manuscript presents important data on the coronary vascular structure of several different species. However, these data alone do not conclusively demonstrate whether the developmental origins of ASV like vessels are homologous. Therefore, care should be taken when concluding that the outflow tract vessels found in all different species are conserved features. While this is a reasonable hypothesis and should be presented, the manuscript could be improved by also discussing alternate explanations. For example, ASVs in mice originate during embryonic development, while in fish and amphibians outflow tract vessels are formed only in mature animals.
We have added data on mice and amphibians (e.g., Fig. 2) and substantially revised the overall development and discussion of the paper. Morphological homology is evident for ASVs and amphibian ASV-like vessels, but the homologous relationship with the hypobranchial artery only suggests a similarity in the embryonic region.
Comparisons of developmental timings of the various structures among diferent lineages of vertebrates reveal that heterochronical shifts are not uncommon. For example, ossification of the head skeleton and vertebrae occurs during the fetal stage in amniotes, but after hatching in larval amphibians and teleosts. A similar trend is observed in the development of the limb bud (paired fins). Overall, the larval stages of amphibians and teleosts are comparable to the fetal stages of amniotes for many structures. We did not suppose this to be particularly unusual, and we did not include it in the text.
- Figure 3 A-D: The authors state that "the ASV ran through the outflow tract, then entered the aortic root before reaching the ventricle to form a secondary orifice". Do the authors have serial sections to conclude that the vessel branching off the carotid runs the length of the aorta and is continuous with an orifice at the aortic root? The endothelial projection off the aorta in panel C could reasonably be an independent projection. For example, Chen et al., described similar looking projections in the base of the aorta that were not attached to external vessels. A whole mount approach would be the most convincing to show the attachments of the ASV vessel.
We added the data of the whole-mount immunohistochemistry. Please refer Figs. 2 and S2.
- Figure 3E: Similar as above, how is it concluded that the orifice is continuous with the ASV and that this projection is not the coronary artery stem?
As for quail, we could not achieve as a clear whole-mount staining as in mice. It was also difficult to trace the route in sections because in quail, ASVs are not restricted to a few lines as in mice, but are the plexus of small vessels. Thus, we added the detailed data from mice (Fig. 2, S2) and we emphasized that the position of orifice in quail is exactly same as that in mice.
- The discussion section could be improved by making some statements more consistent, using more precise or appropriate terminology accepted in the field, and being more cognizant of how the authors' findings fit within the history of the field. For example, when referring to coronary arteries, please clarify whether this refers to ASV/ outflow tract coronary arteries, or true ventricular coronary arteries. In addition, the first sentence of the discussion makes it seem like the origins of coronary arteries were unknown prior to this study, however, their origins have been described in multiple papers previously. The authors could revise their statement to acknowledge these previous findings.
We rewrote the entire text to clarify what each "coronary artery" refers to. We also changed the first section of the discussion as suggested by the reviewer.
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eLife assessment
Mizukami et al. propose a scenario for the evolutionary origin of the coronary artery in amniotes by comparing the morphologies of the vasculatures across several species and developmental timepoints. They show that the coronary arteries of non-amniotes most closely resemble embryonic amniote aortic subepicardial vessels (ASVs), which are replaced by the true coronary arteries during amniote development. While the identification of common vascular structures in diverse taxa is a valuable contribution, additional developmental evidence is needed to confirm that such vessels are truly homologous.
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Reviewer #1 (Public Review):
The authors generated detailed anatomical descriptions and images of the coronary vasculature of mice, quails, zebrafish, Japanese tree frogs, Japanese fire belly newt, African clawed frogs, salmon sharks, Japanese sleeper rays and bird-beak dogfish. Using this data, they are able to show anatomical similarities in the origination points of evolutionary distant vertebrates from the third to fourth brachial arch. Additionally, the authors highlight the additional presence of a coronary vascular plexuses as a unique amniote trait, since it is seen in quail and mice but not xenopus frogs. Based on the presence of the possible homologies, the authors propose that the early developmental amniotic coronary artery is a derived from the ancestral hypobrachial artery. The methods for labeling and imaging the cardiac …
Reviewer #1 (Public Review):
The authors generated detailed anatomical descriptions and images of the coronary vasculature of mice, quails, zebrafish, Japanese tree frogs, Japanese fire belly newt, African clawed frogs, salmon sharks, Japanese sleeper rays and bird-beak dogfish. Using this data, they are able to show anatomical similarities in the origination points of evolutionary distant vertebrates from the third to fourth brachial arch. Additionally, the authors highlight the additional presence of a coronary vascular plexuses as a unique amniote trait, since it is seen in quail and mice but not xenopus frogs. Based on the presence of the possible homologies, the authors propose that the early developmental amniotic coronary artery is a derived from the ancestral hypobrachial artery. The methods for labeling and imaging the cardiac vessels are robust and congruent with previous studies describing these structures in mice and zebrafish. The study also presents an intriguing hypothesis; however, it could benefit from a more expansive survey of vertebrate coronary diversity using an increased number of species and developmental time points. A more exhaustive surveying of vertebrate diversity is required to demonstrate that the coronary vasculature anatomy observed is from common ancestral states or novel adaptations. The author's claim that a primitive vascular plexus represents a novel amniote phenotype, is reasonable, but could benefit from further confirmation using additional species.
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Reviewer #2 (Public Review):
In this manuscript, Mizukami et al. investigate the differences in coronary vasculature morphology across several diverse species to investigate the transition of extrinsic coronary arteries existing on the outflow track in non-amniotes to arteries presenting on the ventricle surface itself in amniotes. They use various visualization techniques, including resin-filling, tissue staining, and fluorescence microscopy to compare the gross morphology and orifice locations of the aortic subepicardial vessels (ASVs) between several amniotes and non-amniotes. Intriguingly, the authors show that the embryonic amniotes rely on a similar ASV structure to adult non-amniotes, but this primitive structure is lost during development in favor of the formation of true coronary arteries on the ventricle surface. While these …
Reviewer #2 (Public Review):
In this manuscript, Mizukami et al. investigate the differences in coronary vasculature morphology across several diverse species to investigate the transition of extrinsic coronary arteries existing on the outflow track in non-amniotes to arteries presenting on the ventricle surface itself in amniotes. They use various visualization techniques, including resin-filling, tissue staining, and fluorescence microscopy to compare the gross morphology and orifice locations of the aortic subepicardial vessels (ASVs) between several amniotes and non-amniotes. Intriguingly, the authors show that the embryonic amniotes rely on a similar ASV structure to adult non-amniotes, but this primitive structure is lost during development in favor of the formation of true coronary arteries on the ventricle surface. While these data intend to show that the difference in coronary artery structure exists between amniotes and non-amniotes, the authors only investigated mice and quail as amniote representatives. Without the inclusion of an ectothermic reptile species as an additional amniote representative, it is entirely possible that the difference in coronary artery structure may instead exist across the endotherm-ectotherm axis as opposed to amniotes and non-amniotes. Despite these concerns, Mizukami et al. show intriguing evolutionary differences between coronary artery structure that draw parallels to changes observed during amniote development.
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Reviewer #3 (Public Review):
Mizukami et al. compare the structure of the coronary arteries in multiple species of amniotes, amphibians, and fish. By selecting species from each of these taxa, the authors were able to evaluate modifications to the coronary arteries during key evolutionary transitions. In mice and quail, they show two populations of vessels that are visible on the developing heart-true coronary arteries on the ventricle and a second population of vessels on the outflow tract known as the ASV., They found that in amphibians, outflow tract vessels were present but ventricular coronary arteries were completely absent. In zebrafish (a more ancestral species) an arterial branch off the rostral section of the hypobranchial artery was shown to have similar anatomical features to outflow tract vessels found in higher organisms. …
Reviewer #3 (Public Review):
Mizukami et al. compare the structure of the coronary arteries in multiple species of amniotes, amphibians, and fish. By selecting species from each of these taxa, the authors were able to evaluate modifications to the coronary arteries during key evolutionary transitions. In mice and quail, they show two populations of vessels that are visible on the developing heart-true coronary arteries on the ventricle and a second population of vessels on the outflow tract known as the ASV., They found that in amphibians, outflow tract vessels were present but ventricular coronary arteries were completely absent. In zebrafish (a more ancestral species) an arterial branch off the rostral section of the hypobranchial artery was shown to have similar anatomical features to outflow tract vessels found in higher organisms. These zebrafish outflow tract arteries also appeared conserved in several chondriichthyes specimens. The authors conclude that rearrangement of the outflow tract vasculature or hypobranchial arteries in fish during evolution, could be homologous to the ASV population of coronary arteries in amphibians and amniotes. These data give new insight into the evolutionary origins of the coronary vasculature.
Major Points
1. The manuscript presents important data on the coronary vascular structure of several different species. However, these data alone do not conclusively demonstrate whether the developmental origins of ASV like vessels are homologous. Therefore, care should be taken when concluding that the outflow tract vessels found in all different species are conserved features. While this is a reasonable hypothesis and should be presented, the manuscript could be improved by also discussing alternate explanations. For example, ASVs in mice originate during embryonic development, while in fish and amphibians outflow tract vessels are formed only in mature animals.
2. Figure 3 A-D: The authors state that "the ASV ran through the outflow tract, then entered the aortic root before reaching the ventricle to form a secondary orifice". Do the authors have serial sections to conclude that the vessel branching off the carotid runs the length of the aorta and is continuous with an orifice at the aortic root? The endothelial projection off the aorta in panel C could reasonably be an independent projection. For example, Chen et al., described similar looking projections in the base of the aorta that were not attached to external vessels. A whole mount approach would be the most convincing to show the attachments of the ASV vessel.
3. Figure 3E: Similar as above, how is it concluded that the orifice is continuous with the ASV and that this projection is not the coronary artery stem?
4. The discussion section could be improved by making some statements more consistent, using more precise or appropriate terminology accepted in the field, and being more cognizant of how the authors' findings fit within the history of the field. For example, when referring to coronary arteries, please clarify whether this refers to ASV/ outflow tract coronary arteries, or true ventricular coronary arteries. In addition, the first sentence of the discussion makes it seem like the origins of coronary arteries were unknown prior to this study, however, their origins have been described in multiple papers previously. The authors could revise their statement to acknowledge these previous findings.
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