Modern research has majorly advanced our understanding of how the heart works, and has led to new therapies for cardiac diseases. However, little is known about how the heart has evolved throughout the history of animals with backbones – a group that is collectively referred to as vertebrates. This is partly because the heart is made from soft muscle tissue, which does not fossilize as often as harder tissues such as bones.

Even though fossils of soft tissues are rare, paleontologists have already unearthed fossils of other soft organs such as the stomach and umbilical cord. These discoveries suggested that there was hope of finding fossil hearts, and now Maldanis, Carvalho et al. have indeed discovered fossil hearts in two specimens of an extinct species of bony fish called Rhacolepis buccalis. These fish were alive over 113 million years ago during the Cretaceous period, in an area that is now modern-day Brazil.

Like all known vertebrates, these R. buccalis fossils have valves between the heart and the major artery that carries blood out of the heart. Such valves are vital because they prevent pumped blood from flowing back into the heart. However, oddly, R. buccalis fossils show five of these valves, which is more than any advanced bony fish that is alive today. Comparing this with the situation in other fish species suggests that vertebrate hearts gradually evolved to become progressively simpler.

This discovery shows that it is possible to study heart evolution with fossils. Maldanis, Carvalho et al. hope that their findings will stimulate researchers from all over the world to examine the fossils of well-preserved animals in search of clues to help reconstruct the major steps in the evolution of the vertebrate heart.

The hearts of ray-finned fishes (actinopterygians) are presently described as a succession of four muscular chambers that perform inflow (sinus venosus and atrium) and outflow (ventricle and conus arteriosus) roles, followed by the bulbus arteriosus, a terminal, non-chambered, elastic cardiac segment (Simões-Costa et al., 2005; Grimes et al., 2006; Durán et al., 2008).

In basal actinopterygians, the conus arteriosus dominates the cardiac outflow, while in teleosts, it is the bulbus arteriosus that prevails, a notion that harks back to Gegenbaur (1866) and before. The conus arteriosus displays multiple fibrous valve rows, a character state that represents the general gnathostome condition, primitively retained in basal actinopterygian groups (Durán et al., 2008; Boas, 1880; Boas, 1901; Schib et al., 2002; Xavier-Neto et al., 2010; Parsons, 1929; Icardo et al., 2002a; Durán et al., 2014; Icardo et al., 2002b). The multiple conal valve rows of basal actinopterygians prevent backflow and protect the delicate gill vessels from the elevated pulsations generated by the ventricle (Satchell and Jones, 1967). In contrast, in derived actinopterygians such as the teleost zebrafish, the valveless bulbus arteriosus protects the gills through its prominent elastic properties (i.e. functioning as a windkessel [Farrell, 1979]). Thus, teleost hearts display only one valve row at the bulbo-ventricular transition, which is now regarded as an evolutionary remnant of the conus arteriosus (Grimes et al., 2006).

The transition from a heart packed with dozens of outflow tract valves in basal actinopterygians, such as in the genus Polypterus (Durán et al., 2014), to the single valve row in the cardiac outflow tract of derived actinopterygians, such as in the cypriniform teleost Danio rerio (the zebrafish) (Grimes and Kirby, 2009) represents a celebrated, hundred-year-old, case of secondary cardiac simplification. The emphasis on the bulbus arteriosus, rather than on the conus arteriosus in teleosts, and the concurrent reduction in the number of outflow valve rows are presently almost completely unconstrained in evolutionary and developmental times. We know that the primitive actinopterygian Polypterus diverged from other actinopterygian lineages (including the zebrafish) by about 390 Mya (Takeuchi et al., 2009) and that the elastic bulbus arteriosus of teleosts represents a very late ontogenetic addition, being added to the heart only after cardiac chambers are formed (Grimes et al., 2006; Grimes and Kirby, 2009). With such limited information, it is impossible to answer whether outflow tract simplification in teleosts represented another case of phyletic gradualism, or resulted from drastic developmental effects. Significant morphological changes are sometimes associated with major genetic changes, such as large-scale gene duplications and/or changes in the function of genes with major developmental effects, both known to have taken place in teleost evolution (Shapiro et al., 2004; Shubin et al., 1997). Knowledge of morphological transitions between character states is critical to the construction of any evolutionary hypothesis. Thus, the first steps toward the understanding of any evolutionary modification ideally involve the discovery of intermediate morphologies.

Unfortunately, there are no universally recognized descriptions of fossilized vertebrate chambered hearts (Xavier-Neto et al., 2010; Janvier, 1996; Rowe et al., 2001; Fisher et al., 2000; Cleland et al., 2011). Although provocative clues accumulate (Janvier, 1996; Rowe et al., 2001; Fisher et al., 2000; Cleland et al., 2011; Shu et al., 2003; Carvalho and Maisey, 1996, Janvier et al., 1991), none of the specimens described so far retained enough original attributes to establish beyond dispute that cardiac preservation is possible. Part of the problem is that the heart is formed by soft tissues, which fossilize only under special conditions (Martill, 1988). However, other soft organs have been described in the Cretaceous of Araripe, Brazil (Martill, 1988; 1990; Pradel et al., 2009; Brito et al., 2010) and even in Paleozoic fishes (380 million-years old) from the Gogo Formation in Australia (Trinajstic et al., 2007; 2013; Long et al., 2008) and Antarctica (Young et al., 2010), which suggests that the difficulty lies not with cardiac preservation, but with the lack of a systematic search.

In the course of a wider search for fossil hearts, we fortuitously found evidence for a long and gradual evolutionary reduction of the conus arteriosus and of its multiple fibrous valve rows in teleosts. The relevant fossils are from the extinct pachyrhizodontid fish Rhacolepis buccalis (Agassiz, 1841), known from fossils of remarkable three-dimensional (3D) preservation (Maisey, 1994). The fossils were collected from the Romualdo Member of the Santana Formation, a Cretaceous Konservat Lagerstätte in the Araripe Basin in the Northeast of Brazil. A pollen and spore-based biostratigraphical analysis indicates a temporal range from 119 to 113 Ma for the strata in which the fossils are found (de Moraes Rios-Netto et al., 2012).

Rhacolepis buccalis is one of the most abundant fishes in the Santana Formation (Maisey, 1991) and belongs to the extinct Mesozoic clade Pachyrhizodontoidei (Arratia, 2008; 2010). The relationships of Pachyrhizodontoidei among teleosts have been disputed (Taverne, 1974; Taverne, 1976; Forey, 1977). There is, however, mounting evidence that some features unite Pachyrhizodontoidei with Elopomorpha (Maisey, 1991) and, recently, Pachyrhizodontoidei, among Crossognathiformes, were placed as a group closely related to Elopomorpha in a basal position among all living teleosts (Arratia, 2008; 2010). Thus, because of its basal phylogenetic position, R. buccalis is well suited for studies on the evolution of morphological characters in teleosts.

Here, we report complete fossil hearts from two R. buccalis specimens (Figure 1). The fossils were scanned with propagation phase contrast synchrotron radiation microtomography (PPC-SR-µCT) at 6 µm resolution The remains of the R. buccalis heart are compressed along the latero-medial axis and were found in an orthotopic position, that is, posterior to gills and between the bones of the pectoral girdle (Figure 1a–b, Video 1). Their cardiac affinity is inferred on the basis of an S-shaped configuration, four chambers (conus arteriosus, ventricle, atrium and sinus venosus), typical ventricular (thick, arrowheads) and atrial (thin, arrows) muscular trabeculae (Figure 1c–f; Video 2), as well as paired Cuvier ducts that join the sinus venosus in the posterior-most region of the heart (not shown).

Figure 1

Download asset Open asset

Video 1

Download asset

Video 2

Download asset

The outflow tract in R. buccalis displays a well-defined conus arteriosus encased by pericardium. Our observations indicate that the R. buccalis conus arteriosus is formed by a thick muscular wall, displays the morphology of a cylinder, which eventually tapers off before joining the aorta at its cranial end and is endowed with multiple valve rows (Figure 1c–d, Video 2, Figure 2). In the region immediately apposed to the heart, the pericardial sac assumes the shape of a pyramid wedged between posterior bilateral gill regions (Video 2). In one of the specimens (CNPEM 17P), the pericardial layer is easily identified near the conal myocardial wall (Figure 2p), while in the other specimen (CNPEM 01P), the limits between the conus arteriosus muscular wall and the pericardium are less marked (Figure 2q). In summary, R. buccalis heart is unique among teleosts in that it displays a large, dominant, conus arteriosus, rather than a predominant bulbus arteriosus in its outflow tract. 

Figure 2

Download asset Open asset

Inside the fossilized conus arteriosus it is possible to discern multiple, nearly parallel layers (Figure 2), which, upon 3D reconstruction, appear disposed as helicoid rings along the cranio-caudal axis of the chamber (Figures 2b,e,h,k,n, Video 3). These structures are interpreted as the fossilized remnants of the fibrous component of individual conal valves, presumably valve leaflets. For comparison, we depict the fibrous components (valve leaflets) of the two conal valves of Megalops atlanticus (Figure 3), a living basal teleost, related to R. buccalis.

Video 3

Download asset

Sagittal and coronal tomographic sections and 3D reconstructions in the two fossil specimens are consistent with the presence of at least five valve rows per conus arteriosus (Figures 2c,f,l,o,p,q). Because of post-mortem changes, of the imperfect alignment of the conus arteriosus to the body axes, and of the semi-lunar character of conal valves (Figure 2), the transverse sections shown in Figure 2 actually represent shallow oblique sections that allow the depiction of more than one valve row per transverse plane (Figure 2b,e,h,k,n), although it is difficult to describe with precision the exact number of valves in each valve row due to the incomplete state of preservation.

Figure 3

Download asset Open asset

One important issue in the study of evolution is the idea of direction, that is, whether natural selection intrinsically favors the emergence of more complex forms or not (McShea, 1996). However, an unequivocal association of evolution with complexity is not a requirement of evolutionary theory (Darwin and Wallace, 1858). Moreover, such a view is at odds with biological evidence of frequent secondary simplifications in the evolution of microorganisms, parasites and in miniaturized/cave/fossorial fishes (Lwoff, 1943; Brusca and Brusca, 2003; Britz et al., 2014). Indeed, cases of morphological simplification reported in the literature most likely represent only a fraction of the examples that falsify the notion that evolution must lead to increased complexity. Many other examples of simplification are found in the evolution of animal circulatory systems (Xavier-Neto et al., 2010; Brusca and Brusca, 2003). Was this the result of traditional phyletic gradualism, or of a saltation event in the wake of large-scale gene duplication (Amores et al., 1998)?

The five rows of conal valves of R. buccalis contrast to the nine valvar rows, each containing three to six individual valves in the basal actinopterygian Polypterus (Durán et al., 2014). Rhacolepis buccalis valves also stand out when compared to the very limited number of conal valves in living teleosts: two valve rows in Elopomorpha (excepting Elops, with one) and a single valve row at the bulbo-ventricular transition in remaining teleosts. Taken together, these two characters, valvar content and overall composition of the R. buccalis heart (i.e. chamber vs. elastic segment), suggest that the outflow tract of this extinct fish represents an intermediate morphology between basal and higher actinopterygians, frozen in time by fossilization as an evolutionary picture taken at the Aptian/Albian boundary, 119–113 Ma (Rios-Netto et al., 2012) (Figures 2 and 3).

Valvar reduction in Actinopterygii was neither seamless, nor restricted to the teleost clade. In fact, acipenseriforms and amiiforms display independent evolutionary tendencies for conus arteriosus simplification and valve reduction when compared to Polypterus. Moreover, among chondrosteans, only acipenseriforms display a clear phenotype of valve reduction, while within holosteans only amiiforms show a reduced number of valves. This suggests that valve reduction happened at least three times independently in actinopterygians (Figure 3).

The five fossil valve rows we describe in R. buccalis indicate that the process of outflow tract simplification involved at least three major transitions at the base of the teleost radiation (around 284 Ma (Betancur et al., 2013; Broughton et al., 2013)): one from nine valve rows to five valve rows (e.g. from Polypterus to R. buccalis); another from five to two valve rows (e.g. from R. buccalis to living elopomorphs); a third to the single outflow valve row retained in all other teleosts (Figure 3b).

It is important to recognize that events other than simplification are also involved in the evolution of the outflow tract in vertebrates. For instance, there is evidence for increase in the number of valves occurring independently in basal Actinopterygii clades, explicitly in Polypteriformes and Lepisosteiformes, which is not illuminated by our present findings.

Figure 4

Download asset Open asset

Currently, it is not possible to ascertain genetic correlates for the valve reduction event in R. buccalis. However, this does not prevent informed speculation that may set parameters for investigation in extant species with longer, or shorter, divergence times from the exuberantly valved Polypterus. In this sense, it is useful to observe that valve reductions in acipenseriforms and amiiforms are uncoupled from the teleost extra round of large-scale genome duplication that may, or may not, have affected R. buccalis. This suggests the possibility that slow, smaller scale, mutational events produced incremental phenotypic changes, which may have been gradually selected for outflow tract simplification in teleosts (Shapiro et al., 2004).

What developmental mechanisms could underlie the transition from conal to bulbal dominance and from valve-rich to single-valved outflow tracts? Although we deal here with outflow composition and number of valve rows as independent characters, it is possible that these traits are not completely independent, and that the relevant parameter is simply the relative extent of outflow tract occupied by the conus arteriosus and its valves, or by the bulbus arteriosus and its valveless, elastic, character (Munoz-Chapuli et al., 1997). Outflow tract variability among actinopterygians was modeled according to Turing’s reaction-diffusion paradigm (Munoz-Chapuli et al., 1997). The major conclusion of this exercise was that the various rows of valves distributed across the cranio-caudal extent of the conus arteriosus and the interspersed valveless spaces can be described as an ensemble of multiple positive and negative domains of endothelial to mesenchymal transformation (Runyan and Markwald, 1983) set up by the interaction between diffusible molecules playing activator and inhibitor roles (Munoz-Chapuli et al., 1997).

The data now available suggest a case of phyletic gradualism, rather than an abrupt saltation-like event for actinopterygian outflow tract simplification. Three lines of evidence support this speculation: evidence for three independent (i.e. convergent) events of valve reduction in Actinopterygii (in acipenseriforms, amiiforms and teleosts); the three valvar simplification steps in teleosts (multiple to five, five to two, and two to one; Figure 4) and the inferred simplicity of developmental mechanisms capable of producing these phenotypes.

The discovery of a fossil heart in R. buccalis demonstrates that systematic, non-destructive approaches can be employed to study cardiovascular evolution and suggests that these sensitive techniques can be utilized not only in the context of species associated with abundant fossils, but also with rare fossils of animals at key phylogenetic positions. Regardless of these specific questions, we hope our results will open exciting new possibilities for research in cardiovascular paleontology and evolution.

1. 1. Agassiz L

   (1841)

   On the fossil fishes found by Mr. Garder in the province of Ceará, in the north of Brazil

   The Edinburgh New Philosophical Journal 30:82–84.

   • Google Scholar
2. 1. Amores A
   2. Force A
   3. Yan YL
   4. Joly L
   5. Amemiya C
   6. Fritz A
   7. Ho RK
   8. Langeland J
   9. Prince V
   10. Wang YL
   11. Westerfield M
   12. Ekker M
   13. Postlethwait JH

   (1998) Zebrafish hox clusters and vertebrate genome evolution

   Science 282:1711–1714.

   https://doi.org/10.1126/science.282.5394.1711

   • Google Scholar
3. 1. Arratia G

   (2008)

   71–92, The varasichthyids and other crossognathiform fishes, and the break-up of Pangaea, London, Fishes and the break-up of Pangaea Special Publication

   71–92, The varasichthyids and other crossognathiform fishes, and the break-up of Pangaea, London, Fishes and the break-up of Pangaea Special Publication.

   • Google Scholar
4. 1. Arratia G

   (2010) The Clupeocephala re-visited: Analysis of characters and homologies

   Revista De Biología Marina Y Oceanografía 45:635–657.

   https://doi.org/10.4067/S0718-19572010000400009

   • Google Scholar
5. 1. Betancur-R. R
   2. Broughton RE
   3. Wiley EO
   4. Carpenter K
   5. López JA
   6. Li C
   7. Holcroft NI
   8. Arcila D
   9. Sanciangco M
   10. Li C
   11. Zhang F
   12. Buser T
   13. Campbell MA
   14. Ballesteros JA
   15. Roa-Varon A
   16. Wiley EO
   17. Borden WC
   18. Rowley T
   19. Li C
   20. Hough DJ
   21. Li C
   22. Grande T
   23. Arratia G
   24. Ortí G

   (2013) The tree of life and a new classification of bony fishes

   PLoS Currents 5:.

   https://doi.org/10.1371/currents.tol.53ba26640df0ccaee75bb165c8c26288

   • Google Scholar
6. 1. Boas JEV

   (1880)

   Über den Conus arteriosus bei Butirinus und bei anderen Knochenfischen

   Morph Jahrb 6:527–534.

   • Google Scholar
7. Book

   1. Boas JEV

   (1901)

   Lehrbuch Der Zoologie

   Jena: G. Fischer.

   • Google Scholar
8. 1. Brito PM
   2. Meunier FJ
   3. Clement G
   4. Geffard-Kuriyama D

   (2010) The histological structure of the calcified lung of the fossil coelacanth Axelrodichthys araripensis (Actinistia: Mawsoniidae)

   Palaeontology 53:1281–1290.

   https://doi.org/10.1111/j.1475-4983.2010.01015.x

   • Google Scholar
9. 1. Britz R
   2. Kakkassery F
   3. Raghavan R

   (2014)

   Osteology of Kryptoglanis shajii, a stygobitic catfish (Teleostei, Siliruformes) from Peninsular India with a diagnosis of the new family Kryptoglanidae

   Ichthyol Explor Freshwaters 24:193–207.

   • Google Scholar
10. 1. Broughton RE
    2. Betancur-R. R
    3. Li C
    4. Arratia G
    5. Ortí G

    (2013) Multi-locus phylogenetic analysis reveals the pattern and tempo of bony fish evolution

    PLoS Currents 5:.

    https://doi.org/10.1371/currents.tol.2ca8041495ffafd0c92756e75247483e

    • Google Scholar
11. Book

    1. Brusca RC
    2. Brusca GJ

    (2003)

    Invertebrates (2nd ed.)

    Sunderland, Mass: Sinauer Associates.

    • Google Scholar
12. Book

    1. Carvalho MRd
    2. Maisey JG

    (1996)

    Phylogenetic relationships of the Late Jurassic shark Protospinax Woodward 1919 (Chondrichthyes: Elasmobranchii)

    In: Arratia G, Viohl G, editors. Mesozoic Fishes - Systematics and Paleoecology. München, Germany: Verlag Dr. Friedrich Pfiel. pp. 9–46.

    • Google Scholar
13. 1. Cleland TP
    2. Stoskopf MK
    3. Schweitzer MH

    (2011) Histological, chemical, and morphological reexamination of the "heart" of a small Late Cretaceous Thescelosaurus

    Die Naturwissenschaften 98:203–211.

    https://doi.org/10.1007/s00114-010-0760-1

    • Google Scholar
14. 1. Danforth CH

    (1912) The heart and arteries of Polyodon

    Journal of Morphology 23:409–454.

    https://doi.org/10.1002/jmor.1050230303

    • Google Scholar
15. 1. Darwin C
    2. Wallace A

    (1858) On the Tendency of Species to form Varieties; and on the Perpetuation of Varieties and Species by Natural Means of Selection

    Journal of the Proceedings of the Linnean Society of London. Zoology 3:45–62.

    https://doi.org/10.1111/j.1096-3642.1858.tb02500.x

    • Google Scholar
16. 1. de Moraes Rios-Netto A
    2. da Silva Pares Regali M
    3. de Souza Carvalho I
    4. Idalécio de Freitas F

    (2012) Palinoestratigrafia do intervalo Alagoas da Bacia do Araripe, Nordeste do Brasil

    Revista Brasileira De Geociências 42:331–342.

    https://doi.org/10.5327/Z0375-75362012000200009

    • Google Scholar
17. 1. Durán AC
    2. Fernández B
    3. Grimes AC
    4. Rodríguez C
    5. Arqué JM
    6. Sans-Coma V

    (2008) Chondrichthyans have a bulbus arteriosus at the arterial pole of the heart: morphological and evolutionary implications

    Journal of Anatomy 213:597–606.

    https://doi.org/10.1111/j.1469-7580.2008.00973.x

    • Google Scholar
18. 1. Durán AC
    2. Reyes-Moya I
    3. Fernández B
    4. Rodríguez C
    5. Sans-Coma V
    6. Grimes AC

    (2014) The anatomical components of the cardiac outflow tract of the gray bichir, Polypterus senegalus: their evolutionary significance

    Zoology 117:370–376.

    https://doi.org/10.1016/j.zool.2014.05.003

    • Google Scholar
19. 1. Farrell AP

    (1979) The Wind-Kessel effect of the bulbus arteriosus in trout

    Journal of Experimental Zoology 209:169–173.

    https://doi.org/10.1002/jez.1402090120

    • Google Scholar
20. 1. Fisher PE
    2. Russell DA
    3. Stoskopf MK
    4. Barrick RE
    5. Hammer M
    6. Kuzmitz AA

    (2000) Cardiovascular evidence for an intermediate or higher metabolic rate in an ornithischian dinosaur

    Science 288:503–505.

    https://doi.org/10.1126/science.288.5465.503

    • Google Scholar
21. Book

    1. Forey PL

    (1977)

    The osteology of Notelops Woodward, Rhacolepis Agassiz and Pachyrhizodus Dixon (Pisces: Teleostei)

    London: Bulletin of the British Museum (Natural History).

    • Google Scholar
22. 1. Gegenbaur C

    (1866)

    Zur vergleichenden Anatomie des Herzens

    Jenaische Zeitschrift Für Medicin Und Naturwissenschaft 2:365–383.

    • Google Scholar
23. 1. Grimes AC
    2. Stadt HA
    3. Shepherd IT
    4. Kirby ML

    (2006) Solving an enigma: arterial pole development in the zebrafish heart

    Developmental Biology 290:265–276.

    https://doi.org/10.1016/j.ydbio.2005.11.042

    • Google Scholar
24. 1. Grimes AC
    2. Kirby ML

    (2009) The outflow tract of the heart in fishes: anatomy, genes and evolution

    Journal of Fish Biology 74:983–1036.

    https://doi.org/10.1111/j.1095-8649.2008.02125.x

    • Google Scholar
25. 1. Icardo JM
    2. Colvee E
    3. Cerra MC
    4. Tota B

    (2002a) The structure of the conus arteriosus of the sturgeon (Acipenser naccarii) heart: II. the myocardium, the subepicardium, and the conus-aorta transition

    The Anatomical Record 268:388–398.

    https://doi.org/10.1002/ar.10170

    • Google Scholar
26. 1. Icardo JM
    2. Colvee E
    3. Cerra MC
    4. Tota B

    (2002b) Structure of the conus arteriosus of the sturgeon (Acipenser naccarii) heart. I: the conus valves and the subendocardium

    Anat Rec 267:17–27.

    https://doi.org/10.1002/ar.10080

    • Google Scholar
27. 1. Janvier P
    2. Percy LR
    3. Potter IC

    (1991) The arrangement of the heart chambers and associated blood vessels in the Devonian osteostracan Norselaspis glacialis. a reinterpretation based on recent studies of the circulatory system in lampreys

    Journal of Zoology 223:567–576.

    https://doi.org/10.1111/j.1469-7998.1991.tb04388.x

    • Google Scholar
28. Book

    1. Janvier P

    (1996)

    Early Vertebrates

    New York: Oxford University Press Inc.

    • Google Scholar
29. 1. Long JA
    2. Trinajstic K
    3. Young GC
    4. Senden T

    (2008) Live birth in the Devonian period

    Nature 453:650–653.

    https://doi.org/10.1038/nature06966

    • Google Scholar
30. Book

    1. Lwoff A

    (1943)

    L'évolution Physiologique. Etude Des Pertes De Fonctions Chez Les Microorganismes

    Paris: Hermann et Cie.

    • Google Scholar
31. Book

    1. Maisey JG

    (1991)

    Santana Fossils: An Illustrated Atlas

    Neptune City: T.F.H. Publications.

    • Google Scholar
32. 1. Maisey JG

    (1994) Predator-prey relationships and trophic level reconstruction in a fossil fish community

    Environmental Biology of Fishes 40:1–22.

    https://doi.org/10.1007/BF00002179

    • Google Scholar
33. 1. Martill DM

    (1988)

    Preservation of fish in the Cretaceous Santana Formation of Brazil

    Paleontology 31:1–18.

    • Google Scholar
34. 1. Martill DM

    (1990) Macromolecular resolution of fossilized muscle tissue from an elopomorph fish

    Nature 346:171–172.

    https://doi.org/10.1038/346171a0

    • Google Scholar
35. 1. McShea DW

    (1996) Perspective: Metazoan complexity and evolution: is there a trend?

    Evolution 50:477–492.

    https://doi.org/10.2307/2410824

    • Google Scholar
36. 1. Munoz-Chapuli R
    2. Gallego A
    3. Perez-Pomares JM

    (1997) A reaction-diffusion model can account for the anatomical pattern of the cardiac conal valves in fish

    Journal of Theoretical Biology 185:233–240.

    https://doi.org/10.1006/jtbi.1996.0303

    • Google Scholar
37. 1. Parsons CW

    (1929)

    The conus arteriosus in fishes

    Quarterly Journal of Microscopical Science 73:145–176.

    • Google Scholar
38. 1. Pradel A
    2. Langer M
    3. Maisey JG
    4. Geffard-Kuriyama D
    5. Cloetens P
    6. Janvier P
    7. Tafforeau P

    (2009) Skull and brain of a 300-million-year-old chimaeroid fish revealed by synchrotron holotomography

    Proceedings of the National Academy of Sciences of the United States of America 106:5224–5228.

    https://doi.org/10.1073/pnas.0807047106

    • Google Scholar
39. 1. Rowe T
    2. McBride EF
    3. Sereno PC

    (2001) Dinosaur with a heart of stone

    Science 291:783a–783.

    https://doi.org/10.1126/science.291.5505.783a

    • Google Scholar
40. 1. Runyan RB
    2. Markwald RR

    (1983) Invasion of mesenchyme into three-dimensional collagen gels: a regional and temporal analysis of interaction in embryonic heart tissue

    Developmental Biology 95:108–114.

    https://doi.org/10.1016/0012-1606(83)90010-6

    • Google Scholar
41. 1. Satchell GH
    2. Jones MP

    (1967)

    The function of the conus arteriosus in the Port Jackson shark, Heterodontus portusjacksoni

    The Journal of Experimental Biology 46:373–382.

    • Google Scholar
42. 1. Schib JL
    2. Icardo JM
    3. Durán AC
    4. Guerrero A
    5. López D
    6. Colvee E
    7. de Andrés AV
    8. Sans-Coma V

    (2002) The conus arteriosus of the adult gilthead seabream (Sparus auratus)

    Journal of Anatomy 201:395–404.

    https://doi.org/10.1046/j.0021-8782.2002.00110.x

    • Google Scholar
43. 1. Senior HD

    (1907)

    Teleosts with a conus having more than one row of valves

    The Anatomical Record 1:83–84.

    • Google Scholar
44. 1. Shapiro MD
    2. Marks ME
    3. Peichel CL
    4. Blackman BK
    5. Nereng KS
    6. Jónsson B
    7. Schluter D
    8. Kingsley DM

    (2004) Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks

    Nature 428:717–723.

    https://doi.org/10.1038/nature02415

    • Google Scholar
45. 1. Shu DG
    2. Morris SC
    3. Han J
    4. Zhang ZF
    5. Yasui K
    6. Janvier P
    7. Chen L
    8. Zhang XL
    9. Liu JN
    10. Li Y
    11. Liu HQ

    (2003) Head and backbone of the Early Cambrian vertebrate Haikouichthys

    Nature 421:526–529.

    https://doi.org/10.1038/nature01264

    • Google Scholar
46. 1. Shubin N
    2. Tabin C
    3. Carroll S

    (1997) Fossils, genes and the evolution of animal limbs

    Nature 388:639–648.

    https://doi.org/10.1038/41710

    • Google Scholar
47. 1. Simões-Costa MS
    2. Vasconcelos M
    3. Sampaio AC
    4. Cravo RM
    5. Linhares VL
    6. Hochgreb T
    7. Yan CY
    8. Davidson B
    9. Xavier-Neto J

    (2005) The evolutionary origin of cardiac chambers

    Developmental Biology 277:1–15.

    https://doi.org/10.1016/j.ydbio.2004.09.026

    • Google Scholar
48. 1. Takeuchi M
    2. Okabe M
    3. Aizawa S

    (2009) The genus Polypterus (bichirs): a fish group diverged at the stem of ray-finned fishes (Actinopterygii)

    Cold Spring Harbor Protocols 2009:pdb.emo117.

    https://doi.org/10.1101/pdb.emo117

    • Google Scholar
49. Book

    1. Taverne L

    (1974)

    L' Ostéologie d'Elops Linné, C., 1766 (Pisces Elopiformes) Et Son Intérêt Phylogénétique. Académie Royale De Belgique. Mémoires. Classe Des Sciences. Col. in 8o, 2ème Série

    Palais des Académies.

    • Google Scholar
50. 1. Taverne L

    (1976)

    À propos du poisson fossile Notelops brama (Agassiz, L. 1841) du Crétacé Inférieur du Brésil et de sa position systematique au sein des Téléostéens primitifs

    Biologisch Jaarboek Dodonaea 44:304–310.

    • Google Scholar
51. 1. Trinajstic K
    2. Marshall C
    3. Long J
    4. Bifield K

    (2007) Exceptional preservation of nerve and muscle tissues in Late Devonian placoderm fish and their evolutionary implications

    Biology Letters 3:197–200.

    https://doi.org/10.1098/rsbl.2006.0604

    • Google Scholar
52. 1. Trinajstic K
    2. Sanchez S
    3. Dupret V
    4. Tafforeau P
    5. Long J
    6. Young G
    7. Senden T
    8. Boisvert C
    9. Power N
    10. Ahlberg PE

    (2013) Fossil musculature of the most primitive jawed vertebrates

    Science 341:160–164.

    https://doi.org/10.1126/science.1237275

    • Google Scholar
53. Book

    1. Xavier-Neto J
    2. Davidson B
    3. Simoes-Costa MS
    4. Castro RA
    5. Castillo HA
    6. Sampaio AC

    (2010)

    Evolutionary Origins of Hearts

    In: Rosenthal N, Harvey RP, editors. Heart Development and Regeneration. London: Elsevier Inc. pp. 3–45.

    • Google Scholar
54. 1. Young GC
    2. Burrow CJ
    3. Long JA
    4. Turner S
    5. Choo B

    (2010) Devonian macrovertebrate assemblages and biogeography of East Gondwana (Australasia, Antarctica)

    Palaeoworld 19:55–74.

    https://doi.org/10.1016/j.palwor.2009.11.005

    • Google Scholar

Author details

1. Lara Maldanis

   1. Department of Pharmacology, University of Campinas, Campinas, Brazil
   2. Brazilian Biosciences National Laboratory, Campinas, Brazil

   Contribution

   LM, Produced acid preparations, rock sections, image segmentations and data integration, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Contributed equally with

   Murilo Carvalho

   Competing interests

   The authors declare that no competing interests exist.

2. Murilo Carvalho

   1. Brazilian Biosciences National Laboratory, Campinas, Brazil
   2. Department of Zoology, Biosciences Institute, University of São Paulo, São Paulo, Brazil

   Contribution

   MC, Geology and Systematic Paleontology, Performed anatomical analyses, Edited figures and reviewed the manuscript, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Contributed equally with

   Lara Maldanis

   Competing interests

   The authors declare that no competing interests exist.

   "This ORCID iD identifies the author of this article:" 0000-0001-6881-5271

3. Mariana Ramos Almeida

   Institute of Chemistry, University of Campinas, Campinas, Brazil

   Contribution

   MRA, Validated initial findings and contributed to discussions and writing, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

4. Francisco Idalécio Freitas

   Geopark Araripe, Crato, Brazil

   Contribution

   FIF, Fieldwork, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

5. José Artur Ferreira Gomes de Andrade

   National Department of Mineral Production, Ministry of Mines and Energy, Crato, Brazil

   Contribution

   JAFGdA, Fieldwork, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

6. Rafael Silva Nunes

   Brazilian Synchrotron Light Laboratory, Campinas, Brazil

   Contribution

   RSN, Validated initial findings and contributed to discussions and writing, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

7. Carlos Eduardo Rochitte

   Heart Institute, InCor, University of São Paulo, São Paulo, Brazil

   Contribution

   CER, CT Scans, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

8. Ronei Jesus Poppi

   Institute of Chemistry, University of Campinas, Campinas, Brazil

   Contribution

   RJP, Validated initial findings and contributed to discussions and writing, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

9. Raul Oliveira Freitas

   Brazilian Synchrotron Light Laboratory, Campinas, Brazil

   Contribution

   ROF, Validated initial findings and contributed to discussions and writing, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

10. Fábio Rodrigues

    Institute of Chemistry, University of São Paulo, São Paulo, Brazil

    Contribution

    FR, Validated initial findings and contributed to discussions and writing, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

    Competing interests

    The authors declare that no competing interests exist.

11. Sandra Siljeström

    Department of Chemistry, Materials, and Surfaces, SP Technical Research Institute of Sweden, Borås, Sweden

    Contribution

    SS, Validated initial findings and contributed to discussions and writing, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

    Competing interests

    The authors declare that no competing interests exist.

12. Frederico Alves Lima

    Brazilian Synchrotron Light Laboratory, Campinas, Brazil

    Contribution

    FAL, Validated initial findings and contributed to discussions and writing, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

    Competing interests

    The authors declare that no competing interests exist.

13. Douglas Galante

    Brazilian Synchrotron Light Laboratory, Campinas, Brazil

    Contribution

    DG, Validated initial findings and contributed to discussions and writing, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

    Competing interests

    The authors declare that no competing interests exist.

14. Ismar S Carvalho

    Departamento de Geologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

    Contribution

    ISC, Fieldwork, Geology and Systematic Paleontology, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

    Competing interests

    The authors declare that no competing interests exist.

    "This ORCID iD identifies the author of this article:" 0000-0002-1811-0588

15. Carlos Alberto Perez

    Brazilian Synchrotron Light Laboratory, Campinas, Brazil

    Contribution

    CAP, Validated initial findings and contributed to discussions and writing, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

    Competing interests

    The authors declare that no competing interests exist.

    "This ORCID iD identifies the author of this article:" 0000-0003-4284-3148

16. Marcelo Rodrigues de Carvalho

    Department of Zoology, Biosciences Institute, University of São Paulo, São Paulo, Brazil

    Contribution

    MRdC, Geology and Systematic Paleontology, Discussed the results, reviewed and contributed to the text, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

    Competing interests

    The authors declare that no competing interests exist.

17. Jefferson Bettini

    Brazilian Nanotechnology National Laboratory, Campinas, Brazil

    Contribution

    JB, Validated initial findings and contributed to discussions and writing, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

    Competing interests

    The authors declare that no competing interests exist.

18. Vincent Fernandez

    European Synchrotron Radiation Facility, Grenoble, France

    Contribution

    VF, PPC-SR-µCT scans and reconstructions, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

    For correspondence

    vincent.fernandez@esrf.fr

    Competing interests

    The authors declare that no competing interests exist.

19. José Xavier-Neto

    Brazilian Biosciences National Laboratory, Campinas, Brazil

    Contribution

    JX-N, Fieldwork, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

    For correspondence

    xavier.neto@lnbio.cnpem.br

    Competing interests

    The authors declare that no competing interests exist.

    "This ORCID iD identifies the author of this article:" 0000-0003-4648-789X

• 6,868

  views

• 1,078

  downloads

• 44

  citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.