1. Ecology
  2. Evolutionary Biology
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Heart fossilization is possible and informs the evolution of cardiac outflow tract in vertebrates

  1. Lara Maldanis
  2. Murilo Carvalho
  3. Mariana Ramos Almeida
  4. Francisco Idalécio Freitas
  5. José Artur Ferreira Gomes de Andrade
  6. Rafael Silva Nunes
  7. Carlos Eduardo Rochitte
  8. Ronei Jesus Poppi
  9. Raul Oliveira Freitas
  10. Fábio Rodrigues
  11. Sandra Siljeström
  12. Frederico Alves Lima
  13. Douglas Galante
  14. Ismar S Carvalho
  15. Carlos Alberto Perez
  16. Marcelo Rodrigues de Carvalho
  17. Jefferson Bettini
  18. Vincent Fernandez  Is a corresponding author
  19. José Xavier-Neto  Is a corresponding author
  1. University of Campinas, Brazil
  2. Brazilian Biosciences National Laboratory, Brazil
  3. University of São Paulo, Brazil
  4. Geopark Araripe, Brazil
  5. Ministry of Mines and Energy, Brazil
  6. Brazilian Synchrotron Light Laboratory, Brazil
  7. SP Technical Research Institute of Sweden, Sweden
  8. Universidade Federal do Rio de Janeiro, Brazil
  9. Brazilian Nanotechnology National Laboratory, Brazil
  10. European Synchrotron Radiation Facility, France
Research Article
Cite this article as: eLife 2016;5:e14698 doi: 10.7554/eLife.14698
4 figures and 3 videos

Figures

Phase contrast synchrotron micro tomography of teleost fossil hearts.

(a,b) 3D reconstructions of specimen CNPEM 27P obtained from PPC-SR-μCT. (a), Left lateral view. (b), Ventral view. (c,d), (e,f) Sagittal sections of specimens CNPEM 01P and CNPEM 17P, respectively. Blue masks in (d) and (f) highlight fossil cardiac chambers and pericardium in the specimens CNPEM 01P and CNPEM 17P, respectively. Note that thin trabeculae are associated to the atrium (arrows) and that thick trabeculae are typical of the ventricle (arrowheads) Abbreviations: A, atrium; C.A., conus arteriosus; P, pericardium; S.V., sinus venosus; V, ventricle.

https://doi.org/10.7554/eLife.14698.003
The fossil conus arteriosus of Rhacolepis buccalis. 

(a-c) Coronal, transversal and sagittal sections of the conus arteriosus of specimen CNPEM 17P taken by Phase contrast synchrotron microtomography (PPC-SR-µCT), respectively. Arrowheads in (c) indicate five conal valve rows in sagittal perspective. (d-f), Drawings of sections in (a-c) highlight conal valve rows (gray). (g-i) Didactic scheme to indicate the orientation of individual valve rows along the three orthogonal body planes (a-c) and (j-l), (j-l) Coronal, transversal and sagittal sections of the conus arteriosus of specimen CNPEM 01P taken by PPC-SR-µCT. Arrowheads in (l) indicate five individual conal valves in sagittal perspective. (m-o) Drawings of sections in (j-l) represent conal valves (gray). (p-q), 3D reconstruction and segmentation of conal valves from specimens CNPEM 01P and 17P, respectively. Note that the pericardium (pink) outlines the conus arteriosus (p). Each individual conal valve is represented by a specific spectral color.

https://doi.org/10.7554/eLife.14698.006
The heart of the extant elopiform Megalops atlanticus with a focus on its outflow tract.

(a) Dissected heart of M. atlanticus. (b) The M. atlanticus heart was cut open along the sagittal plane to expose right and left components of the two conus arteriosus valves. (c) Magnification of the conus arteriosus in (b) showing valve leaflets from the two valve rows (white arrowheads) and the endocardial surface overlying conus arteriosus muscles (black arrows). (d) Scheme representing the right valve leaflets from the conus arteriosus of M. atlanticus as displayed in (c). (e) 3D reconstruction and segmentation of conal valves (blue) superimposed on a M. atlanticus Magnetic Resonance Imaging (MRI). (f) Detail of (e). (g) MRI of the M. atlanticus outflow tract, highlighting two conal valves (arrowheads). Abbreviations: A, atrium; AO., aorta; B, bulbus arteriosus; C.A.; conus arteriosus; L, left side; R, right side; S.V., sinus venosus; V, ventricle.

https://doi.org/10.7554/eLife.14698.008
The Rhacolepis buccalis conus arteriosus is morphologically intermediate in actinopterygian cardiac outflow tract evolution.

(a) Hypothetical transition from a character state composed by an array of multiple valve rows in the conus arteriosus of basal actinopterygians, such as Polypteriformes (top), to a derived state characterized by the dominance of the valveless bulbus arteriosus, in living teleosts (here represented by a generalized elopomorph at the bottom), through an intermediate state represented in the conus arteriosus of fossilized R. buccalis hearts (middle). Anterior to left. (b) Cladogram depicting phylogenetic relationships among early and derived gnathostomes and their corresponding morphologies of the cardiac outflow region. Drawings represent either the inner sides of right (R) and left (L) counterparts, or only the inner right side of the cardiac outflow tract. Drawings were modified from classic illustrations (Parsons, 1929; Danforth, 1912; Senior, 1907) (not to scale). Blue and pink coloring highlight, respectively, bulbus and conus arteriosus (and respective valves) in extant species. Valvar arrangement in Rhacolepis is suggested by data in Figure 2. A parsimony ancestral character state reconstruction was made for the number of conal valves, following the color code in terminals. General relationships of Teleostei were based on Arratia, 2010. Genera illustrating the conal condition in each Actionopterygian branches are: Squalus for Chondrichthyes; Neoceratodus for Sarcopterygii; Polypterus for Polypteriformes; Lepisosteus for Lepisosteiformes; Amia for Amiiformes; Pterothrissus for Albuliformes; Gadus for Clupeocephala. Abbreviations: B, bulbus; C.A., conus arteriosus; L, left side; P, pericardium; R, right side; VE, ventricle.

https://doi.org/10.7554/eLife.14698.009

Videos

Video 1
3D reconstruction of Rhacolepis buccalis CNPEM 27P PPC-SR-μCT.

Animated rotation of the whole specimen zooming at heart position.

https://doi.org/10.7554/eLife.14698.004
Video 2
Rhacolepis buccalis PPC-SR-μCT.

Details of tomography at the heart region and 3D reconstruction of the conal valves.

https://doi.org/10.7554/eLife.14698.005
Video 3
Rhacolepis buccalis PPC-SR-μCT.

Sections of conal valve.

https://doi.org/10.7554/eLife.14698.007

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