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Which came first, the lung or the breath?

Identifieur interne : 001140 ( Istex/Corpus ); précédent : 001139; suivant : 001141

Which came first, the lung or the breath?

Auteurs : Steven F. Perry ; Richard J. A Wilson ; Christian Straus ; Michael B. Harris ; John E. Remmers

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RBID : ISTEX:6932AB6181DDB4CFFFC75C4AA3F1FB552CB77120

English descriptors

Abstract

Lungs are the characteristic air-filled organs (AO) of the Polypteriformes, lungfish and tetrapods, whereas the swimbladder is ancestral in all other bony fish. Lungs are paired ventral derivatives of the pharynx posterior to the gills. Their respiratory blood supply is the sixth branchial artery and the venous outflow enters the heart separately from systemic and portal blood at the sinus venosus (Polypteriformes) or the atrium (lungfish), or is delivered to a separate left atrium (tetrapods). The swimbladder, on the other hand, is unpaired, and arises dorsally from the posterior pharynx. It is employed in breathing in Ginglymodi (gars), Halecomorphi (bowfin) and in basal teleosts. In most cases, its respiratory blood supply is homologous to that of the lung, but the vein drains to the cardinal veins. Separate intercardiac channels for oxygenated and deoxygenated blood are lacking. The question of the homology of lungs and swimbladders and of breathing mechanisms remains open. On the whole, air ventilatory mechanisms in the actinopterygian lineage are similar among different groups, including Polypteriformes, but are distinct from those of lungfish and tetrapods. However, there is extreme variation within this apparent dichotomy. Furthermore, the possible separate origin of air breathing in actinopterygian and ‘sarcopterygian’ lines is in conflict with the postulated much more ancient origin of vertebrate air-breathing organs. New studies on the isolated brainstem preparation of the gar (Lepisosteus osseus) show a pattern of efferent activity associated with a glottal opening that is remarkably similar to that seen in the in-vitro brainstem preparation of frogs and tadpoles. Given the complete lack of evidence for AO in chondrichthyans, and the isolated position of placoderms for which buoyancy organs of uncertain homology have been demonstrated, it is likely that homologous pharyngeal AO arose in the ancestors of early bony fish, and was pre-dated by behavioral mechanisms for surface (water) breathing. The primitive AO may have been the posterior gill pouches or even the modified gills themselves, served by the sixth branchial artery. Further development of the dorsal part may have led to the respiratory swimbladder, whereas the paired ventral parts evolved into lungs.

Url:
DOI: 10.1016/S1095-6433(01)00304-X

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ISTEX:6932AB6181DDB4CFFFC75C4AA3F1FB552CB77120

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<div type="abstract" xml:lang="en">Lungs are the characteristic air-filled organs (AO) of the Polypteriformes, lungfish and tetrapods, whereas the swimbladder is ancestral in all other bony fish. Lungs are paired ventral derivatives of the pharynx posterior to the gills. Their respiratory blood supply is the sixth branchial artery and the venous outflow enters the heart separately from systemic and portal blood at the sinus venosus (Polypteriformes) or the atrium (lungfish), or is delivered to a separate left atrium (tetrapods). The swimbladder, on the other hand, is unpaired, and arises dorsally from the posterior pharynx. It is employed in breathing in Ginglymodi (gars), Halecomorphi (bowfin) and in basal teleosts. In most cases, its respiratory blood supply is homologous to that of the lung, but the vein drains to the cardinal veins. Separate intercardiac channels for oxygenated and deoxygenated blood are lacking. The question of the homology of lungs and swimbladders and of breathing mechanisms remains open. On the whole, air ventilatory mechanisms in the actinopterygian lineage are similar among different groups, including Polypteriformes, but are distinct from those of lungfish and tetrapods. However, there is extreme variation within this apparent dichotomy. Furthermore, the possible separate origin of air breathing in actinopterygian and ‘sarcopterygian’ lines is in conflict with the postulated much more ancient origin of vertebrate air-breathing organs. New studies on the isolated brainstem preparation of the gar (Lepisosteus osseus) show a pattern of efferent activity associated with a glottal opening that is remarkably similar to that seen in the in-vitro brainstem preparation of frogs and tadpoles. Given the complete lack of evidence for AO in chondrichthyans, and the isolated position of placoderms for which buoyancy organs of uncertain homology have been demonstrated, it is likely that homologous pharyngeal AO arose in the ancestors of early bony fish, and was pre-dated by behavioral mechanisms for surface (water) breathing. The primitive AO may have been the posterior gill pouches or even the modified gills themselves, served by the sixth branchial artery. Further development of the dorsal part may have led to the respiratory swimbladder, whereas the paired ventral parts evolved into lungs.</div>
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<note type="content">Fig. 1: The ‘lungs’ of Bothriolepis canadensis. Gi: gill arch; ‘Gl’: glottis; ‘Lu’: lung; Spi: spiral gut. After Denison (1941).</note>
<note type="content">Fig. 2: Wall structure (A,B,C,E,F,G) or solid casts (D,H,) of developmental stages of the pharyngeal pouches of a skate (Torpedo) (A,B,E,F), a sturgeon (Acipenser) (C,G,) and a gymnophion amphibian (Hypogeophis) (D,H), showing the fate of the seventh and eighth pouches. Note the disappearance of the eighth pouch in the skate, the formation of unpaired swimbladder from the dorsal pharyngeal ridge in the sturgeon and the pseudotrachea in the gymnophion amphibian, which is formed by the elongation of the pharyngeal region. (From Perry, 1989, after various sources). Upper row, early developmental stage, lower row, later stage in the same species. Numbers denote gill pouches. Abbreviations: dl, dorsolateral; dm, dorsomedial; Es, esophagus; Lu, lung; med, median ridge; Sb, swimbladder; St, stomach.</note>
<note type="content">Fig. 3: Generalized diagram of the ontogeny of the posterior pharyngeal cavity, based upon Acipenser. Compare with Fig. 2G. Numbers denote the pharyngeal pouch, beginning at the spiracle (s). Abbreviations: d, dorsal; dl, dorsolateral; dm, dorsomedial; v, ventral, vl, ventrolateral. After Wassnetzov (1932).</note>
<note type="content">Fig. 4: Summary of sequence in the evolution of mechanisms (italics) and organs (boldface) air breathing. Black field symbolically indicates the effect of sequentially including the location of the pneumatic foramen, arterial supply and air breathing oscillator. Colors: Blue, ductus cuvieri, cardinal veins and sinus venosus; pink, aortic arches; red, ‘pulmonary’ arteries; green, ‘pulmonary’ veins. Sources of sketches: Denison (1941), Goodrich (1930), Kardong (1998), Wilson et al., (2000). Cladogram from Kardong (1998), based on Liem (1988).</note>
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<p>Lungs are the characteristic air-filled organs (AO) of the Polypteriformes, lungfish and tetrapods, whereas the swimbladder is ancestral in all other bony fish. Lungs are paired ventral derivatives of the pharynx posterior to the gills. Their respiratory blood supply is the sixth branchial artery and the venous outflow enters the heart separately from systemic and portal blood at the sinus venosus (Polypteriformes) or the atrium (lungfish), or is delivered to a separate left atrium (tetrapods). The swimbladder, on the other hand, is unpaired, and arises dorsally from the posterior pharynx. It is employed in breathing in Ginglymodi (gars), Halecomorphi (bowfin) and in basal teleosts. In most cases, its respiratory blood supply is homologous to that of the lung, but the vein drains to the cardinal veins. Separate intercardiac channels for oxygenated and deoxygenated blood are lacking. The question of the homology of lungs and swimbladders and of breathing mechanisms remains open. On the whole, air ventilatory mechanisms in the actinopterygian lineage are similar among different groups, including Polypteriformes, but are distinct from those of lungfish and tetrapods. However, there is extreme variation within this apparent dichotomy. Furthermore, the possible separate origin of air breathing in actinopterygian and ‘sarcopterygian’ lines is in conflict with the postulated much more ancient origin of vertebrate air-breathing organs. New studies on the isolated brainstem preparation of the gar (Lepisosteus osseus) show a pattern of efferent activity associated with a glottal opening that is remarkably similar to that seen in the in-vitro brainstem preparation of frogs and tadpoles. Given the complete lack of evidence for AO in chondrichthyans, and the isolated position of placoderms for which buoyancy organs of uncertain homology have been demonstrated, it is likely that homologous pharyngeal AO arose in the ancestors of early bony fish, and was pre-dated by behavioral mechanisms for surface (water) breathing. The primitive AO may have been the posterior gill pouches or even the modified gills themselves, served by the sixth branchial artery. Further development of the dorsal part may have led to the respiratory swimbladder, whereas the paired ventral parts evolved into lungs.</p>
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<ce:textfn>Review</ce:textfn>
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<ce:title>Which came first, the lung or the breath?</ce:title>
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<ce:author>
<ce:given-name>Steven F</ce:given-name>
<ce:surname>Perry</ce:surname>
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<ce:sup>b</ce:sup>
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<ce:e-address>perry@uni-bonn.de</ce:e-address>
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<ce:surname>Wilson</ce:surname>
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<ce:sup>b</ce:sup>
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<ce:given-name>Christian</ce:given-name>
<ce:surname>Straus</ce:surname>
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<ce:sup>b</ce:sup>
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<ce:sup>c</ce:sup>
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<ce:sup>b</ce:sup>
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<ce:textfn>Institut für Zoologie, Universität Bonn, Poppelsdorfer Schloss, 53115 Bonn, Germany</ce:textfn>
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<ce:affiliation id="AFF2">
<ce:label>b</ce:label>
<ce:textfn>Respiratory Research Group, University of Calgary, Calgary, AB T2N 4N1, Canada</ce:textfn>
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<ce:label>c</ce:label>
<ce:textfn>G.-H. Pitie-Salpetriere, 75651 Paris Cedex 13, France</ce:textfn>
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<ce:label>*</ce:label>
<ce:text>Corresponding author. Tel.: +49-228-733807; fax: +49-228-735458</ce:text>
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<ce:simple-para>Lungs are the characteristic air-filled organs (AO) of the Polypteriformes, lungfish and tetrapods, whereas the swimbladder is ancestral in all other bony fish. Lungs are paired ventral derivatives of the pharynx posterior to the gills. Their respiratory blood supply is the sixth branchial artery and the venous outflow enters the heart separately from systemic and portal blood at the sinus venosus (Polypteriformes) or the atrium (lungfish), or is delivered to a separate left atrium (tetrapods). The swimbladder, on the other hand, is unpaired, and arises dorsally from the posterior pharynx. It is employed in breathing in Ginglymodi (gars), Halecomorphi (bowfin) and in basal teleosts. In most cases, its respiratory blood supply is homologous to that of the lung, but the vein drains to the cardinal veins. Separate intercardiac channels for oxygenated and deoxygenated blood are lacking. The question of the homology of lungs and swimbladders and of breathing mechanisms remains open. On the whole, air ventilatory mechanisms in the actinopterygian lineage are similar among different groups, including Polypteriformes, but are distinct from those of lungfish and tetrapods. However, there is extreme variation within this apparent dichotomy. Furthermore, the possible separate origin of air breathing in actinopterygian and ‘sarcopterygian’ lines is in conflict with the postulated much more ancient origin of vertebrate air-breathing organs. New studies on the isolated brainstem preparation of the gar (
<ce:italic>Lepisosteus osseus</ce:italic>
) show a pattern of efferent activity associated with a glottal opening that is remarkably similar to that seen in the in-vitro brainstem preparation of frogs and tadpoles. Given the complete lack of evidence for AO in chondrichthyans, and the isolated position of placoderms for which buoyancy organs of uncertain homology have been demonstrated, it is likely that homologous pharyngeal AO arose in the ancestors of early bony fish, and was pre-dated by behavioral mechanisms for surface (water) breathing. The primitive AO may have been the posterior gill pouches or even the modified gills themselves, served by the sixth branchial artery. Further development of the dorsal part may have led to the respiratory swimbladder, whereas the paired ventral parts evolved into lungs.</ce:simple-para>
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<ce:text>Lung</ce:text>
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<ce:keyword>
<ce:text>Gill</ce:text>
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<ce:keyword>
<ce:text>Respiratory mechanisms</ce:text>
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<ce:text>Air breathing</ce:text>
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<ce:text>Fish</ce:text>
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<ce:keyword>
<ce:text>Swim bladder</ce:text>
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<ce:keyword>
<ce:text>Evolution</ce:text>
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<abstract lang="en">Lungs are the characteristic air-filled organs (AO) of the Polypteriformes, lungfish and tetrapods, whereas the swimbladder is ancestral in all other bony fish. Lungs are paired ventral derivatives of the pharynx posterior to the gills. Their respiratory blood supply is the sixth branchial artery and the venous outflow enters the heart separately from systemic and portal blood at the sinus venosus (Polypteriformes) or the atrium (lungfish), or is delivered to a separate left atrium (tetrapods). The swimbladder, on the other hand, is unpaired, and arises dorsally from the posterior pharynx. It is employed in breathing in Ginglymodi (gars), Halecomorphi (bowfin) and in basal teleosts. In most cases, its respiratory blood supply is homologous to that of the lung, but the vein drains to the cardinal veins. Separate intercardiac channels for oxygenated and deoxygenated blood are lacking. The question of the homology of lungs and swimbladders and of breathing mechanisms remains open. On the whole, air ventilatory mechanisms in the actinopterygian lineage are similar among different groups, including Polypteriformes, but are distinct from those of lungfish and tetrapods. However, there is extreme variation within this apparent dichotomy. Furthermore, the possible separate origin of air breathing in actinopterygian and ‘sarcopterygian’ lines is in conflict with the postulated much more ancient origin of vertebrate air-breathing organs. New studies on the isolated brainstem preparation of the gar (Lepisosteus osseus) show a pattern of efferent activity associated with a glottal opening that is remarkably similar to that seen in the in-vitro brainstem preparation of frogs and tadpoles. Given the complete lack of evidence for AO in chondrichthyans, and the isolated position of placoderms for which buoyancy organs of uncertain homology have been demonstrated, it is likely that homologous pharyngeal AO arose in the ancestors of early bony fish, and was pre-dated by behavioral mechanisms for surface (water) breathing. The primitive AO may have been the posterior gill pouches or even the modified gills themselves, served by the sixth branchial artery. Further development of the dorsal part may have led to the respiratory swimbladder, whereas the paired ventral parts evolved into lungs.</abstract>
<note type="content">Section title: Review</note>
<note type="content">Fig. 1: The ‘lungs’ of Bothriolepis canadensis. Gi: gill arch; ‘Gl’: glottis; ‘Lu’: lung; Spi: spiral gut. After Denison (1941).</note>
<note type="content">Fig. 2: Wall structure (A,B,C,E,F,G) or solid casts (D,H,) of developmental stages of the pharyngeal pouches of a skate (Torpedo) (A,B,E,F), a sturgeon (Acipenser) (C,G,) and a gymnophion amphibian (Hypogeophis) (D,H), showing the fate of the seventh and eighth pouches. Note the disappearance of the eighth pouch in the skate, the formation of unpaired swimbladder from the dorsal pharyngeal ridge in the sturgeon and the pseudotrachea in the gymnophion amphibian, which is formed by the elongation of the pharyngeal region. (From Perry, 1989, after various sources). Upper row, early developmental stage, lower row, later stage in the same species. Numbers denote gill pouches. Abbreviations: dl, dorsolateral; dm, dorsomedial; Es, esophagus; Lu, lung; med, median ridge; Sb, swimbladder; St, stomach.</note>
<note type="content">Fig. 3: Generalized diagram of the ontogeny of the posterior pharyngeal cavity, based upon Acipenser. Compare with Fig. 2G. Numbers denote the pharyngeal pouch, beginning at the spiracle (s). Abbreviations: d, dorsal; dl, dorsolateral; dm, dorsomedial; v, ventral, vl, ventrolateral. After Wassnetzov (1932).</note>
<note type="content">Fig. 4: Summary of sequence in the evolution of mechanisms (italics) and organs (boldface) air breathing. Black field symbolically indicates the effect of sequentially including the location of the pneumatic foramen, arterial supply and air breathing oscillator. Colors: Blue, ductus cuvieri, cardinal veins and sinus venosus; pink, aortic arches; red, ‘pulmonary’ arteries; green, ‘pulmonary’ veins. Sources of sketches: Denison (1941), Goodrich (1930), Kardong (1998), Wilson et al., (2000). Cladogram from Kardong (1998), based on Liem (1988).</note>
<note type="content">Table 1: Respiratory swimbladders and lungs of fish and tetrapodsa</note>
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<topic>Lung</topic>
<topic>Gill</topic>
<topic>Respiratory mechanisms</topic>
<topic>Air breathing</topic>
<topic>Fish</topic>
<topic>Swim bladder</topic>
<topic>Evolution</topic>
<topic>Functional morphology</topic>
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