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Pulmonary Transformations of Vertebrates

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The Biology of the Avian Respiratory System

Abstract

The structure of the lung subserves its function, which is primarily gas exchange, and selection for expanded capacities for gas exchange is self-evident in the great diversity of pulmonary morphologies observed in different vertebrate lineages. However, expansion of aerobic capacities does not explain all of this diversity, leaving the functional underpinnings of some of the most fascinating transformations of the vertebrate lung unknown. One of these transformations is the evolution of highly branched conducting airways, particularly those of birds and mammals. Birds have an extraordinarily complex circuit of airways through which air flows in the same direction during both inspiration and expiration, unidirectional flow. Mammals also have an elaborate system of conducting airways; however, the tubes arborize rather than form a circuit, and airflow is tidal along the branches of the bronchial tree. The discovery of unidirectional airflow in crocodilians and lizards indicates that several inveterate hypotheses for the selective drivers of this trait cannot be correct. Neither endothermy nor athleticism drove the evolution of unidirectional flow. These discoveries open an uncharted area for research into selective underpinning of unidirectional airflow.

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References

  • Akester A. The comparative anatomy of the respiratory pathways in the domestic fowl (Gallus domesticus), pigeon (Columba livia) and domestic duck (Anas platyrhyncha). J Anat. 1960;4:487–505.

    Google Scholar 

  • Angrist SW. Fluid control devides. Sci Am. 1964;211:80–8.

    Article  Google Scholar 

  • Bethe A. Atmung: Allgemeines und Vergleichendes. In: Bethe A, Bergmann EG, editors. Handbuch der normals und pathologischen Physiology, vol. 2. Berlin: Springer; 1925. p. 1–36.

    Chapter  Google Scholar 

  • Boucot A, Janis C. Environment of the early Paleozoic vertebrates. Palaeogeogr Palaeoclimatol Palaeoecol. 1983;41:251–87.

    Article  Google Scholar 

  • Brackenbury JH. Airflow dynamics in the avian lung as determined by direct and indirect methods. Respir Physiol. 1971;13:318–29.

    Article  Google Scholar 

  • Brackenbury JH. Ventilation of the lung-air sac system. In: Seller TJ, editor. Bird respiration, vol. II. Boca Raton, FL: CRC Press; 1987. p. 39–69.

    Google Scholar 

  • Brainerd EL, Owerkowicz T. Functional morphology and evolution of aspiration breathing in tetrapods. Respir Physiol Neurobiol. 2006;154:73–88.

    Article  PubMed  Google Scholar 

  • Butler G. On the complete or partial suppression of the right lung in the Amphisbaenidae and the left lung in snakes and snake-like lizards and amphibians. Proc Zool Soc Lond. 1895;1895:691–712.

    Google Scholar 

  • Butler JP, Banzett RB, Fredberg JJ. Inspiratory valving in avian bronchi: aerodynamic considerations. Respir Physiol. 1988;72:241–56.

    Article  CAS  PubMed  Google Scholar 

  • Cass AN, Servetnick MD, McCune AR. Expression of a lung developmental cassette in the adult and developing zebrafish swimbladder. Evol Dev. 2013;15:119–32.

    Article  CAS  PubMed  Google Scholar 

  • Cieri RL, Craven BA, Schachner ER, Farmer CG. New insight into the evolution of the vertebrate respiratory system and the discovery of unidirectional airflow in iguana lungs. Proc Natl Acad Sci USA. 2014;111:17218–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coiter V. Anatomie Avium. In Externarum et internarum praecipalium humani corporis partium tabulae atque anatomicae exercitationes observationesque varieae. Germany: Norimbergae; 1573. p. 130–3.

    Google Scholar 

  • Cupello C, Brito PM, Herbin M, Meunier FJ, Janvier P, Dutel H, Clément G. Allometric growth in the extant coelacanth lung during ontogenetic development. Nat Commun. 2015;6:8222.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Darwin C. The descent of man, and selection in relation to sex. London: John Murray; 1871.

    Book  Google Scholar 

  • Dotterweich H. Die Atmung der Vögel. Z f vergl Physiol. 1936;23:744–70.

    Article  Google Scholar 

  • Duncker HR. The lung air sac system of birds. A contribution to the functional anatomy of the respiratory apparatus. Ergeb Anat Entwicklungsgesch. 1971;45:1–171.

    Google Scholar 

  • Duncker HR. General morphological principles of amniotic lungs. In: Piiper J, editor. Respiratory function in birds. Heidelberg: Springer; 1978.

    Google Scholar 

  • Farmer C. Did lungs and the intracardiac shunt evolve to oxygenate the heart in vertebrates? Paleobiology. 1997;23:358–72.

    Article  Google Scholar 

  • Farmer CG. The provenance of alveolar and parabronchial lungs: insights from paleoecology and the discovery of cardiogenic, unidirectional airflow in the American alligator (Alligator mississippiensis). Physiol Biochem Zool. 2010;83:561–75.

    Article  CAS  PubMed  Google Scholar 

  • Farmer CG. On the evolution of vascular patterns of tetrapods. J Morphol. 2011;272:1325–41.

    Article  CAS  PubMed  Google Scholar 

  • Farmer CG. The evolution of unidirectional pulmonary airflow. Physiology. 2015a;30:260–72.

    Article  CAS  PubMed  Google Scholar 

  • Farmer CG. Similarity of crocodilian and avian lungs indicates unidirectional flow is ancestral for archosaurs. Integr Comp Biol. 2015b;55:962–71.

    CAS  PubMed  Google Scholar 

  • Farmer CG, Carrier DR. Pelvic aspiration in the American alligator (Alligator mississippiensis). J Exp Biol. 2000;203:1679–87.

    CAS  PubMed  Google Scholar 

  • Farmer CG, Sanders K. Unidirectional airflow in the lungs of alligators. Science. 2010;327:338–40.

    Article  CAS  PubMed  Google Scholar 

  • Gans C, Clark B. Studies on ventilation of Caiman crocodilus (Crocodilia: Reptilia). Respir Physiol. 1976;26:285–301.

    Article  CAS  PubMed  Google Scholar 

  • Greenblatt EE, Butler JP, Venegas JG, Winkler T. Pendelluft in the bronchial tree. J Appl Physiol. 2014;117:979–88.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hazelhoff EH. Structure and function of the lung of birds. Poult Sci. 1951;30:3–10.

    Article  Google Scholar 

  • Heraty KB, Laffey JG, Quinlan NJ. Fluid dynamics of gas exchange in high-frequency oscillatory ventilation: in vitro investigations in idealized and anatomically realistic airway bifurcation models. Ann Biomed Eng. 2008;36:1856–69.

    Article  PubMed  Google Scholar 

  • Hsia CCW, Schmitz A, Lambertz M, Perry SF, Maina JN. Evolution of air breathing: oxygen homeostasis and the transitions from water to land and sky. Compr Physiol. 2013;3:849–915.

    PubMed  PubMed Central  Google Scholar 

  • Huxley TH. On the respiratory organs of Apteryx. Proc Zool Soc Lond. 1882;1882:560–9.

    Google Scholar 

  • Kramer DL, Lindsey CC, Moodie GEE, Stevens ED. The fishes and the aquatic environment of the central Amazon basin, with particular reference to respiratory patterns. Can J Zool. 1978;56:717–29.

    Article  Google Scholar 

  • Krefft G. Description of a gigantic amphibian allied to genus Lepidosiren, from Wide Bay district, Queensland. Proc Zool Soc Lond. 1870;1870:221–4.

    Google Scholar 

  • Liem KF. Respiratory gas bladders in teleosts: functional conservatism and morphological diversity. Am Zool. 1989;29:333–52.

    Article  Google Scholar 

  • Longo S, Riccio M, McCune AR. Homology of lungs and gas bladders: insights from arterial vasculature. J Morphol. 2013;274:687–703.

    Article  PubMed  Google Scholar 

  • Maina JN. The morphometry of the avian lung. In: King AS, McLelland J, editors. Form and function in birds, vol. 4. London: Academic; 1989. p. 307–68.

    Google Scholar 

  • Maina JN. The gas exchangers: structure, function, and evolution of the respiratory processes. New York: Springer; 1998.

    Book  Google Scholar 

  • Maina JN. What it takes to fly: the structural and functional respiratory refinements in birds and bats. J Exp Biol. 2000;203:3045–64.

    CAS  PubMed  Google Scholar 

  • Maina JN. Some recent advances on the study and understanding of the functional design of the avian lung: morphological and morphometric perspectives. Biol Rev Camb Philos Soc. 2002;77:97–152.

    Article  CAS  PubMed  Google Scholar 

  • Maina JN. Development, structure, and function of a novel respiratory organ, the lung-air sac system of birds: to go where no other vertebrate has gone. Biol Rev Camb Philos Soc. 2006;81:545–79.

    Article  PubMed  Google Scholar 

  • Maina JN, King AS, Settle G. An allometric study of pulmonary morphometric parameters in birds, with mammalian comparisons. Philos Trans R Soc Lond Ser B Biol Sci. 1989;326:1–57.

    Article  CAS  Google Scholar 

  • Maina JN, Veltcamp CJ, Henry J. Study of the spatial organization of the gas exchange components of the snake lung-the sandboa Eryx colubrinus (Reptilia: Ophidia: Colubridae)-by latex casting. J Zool. 1999;247:81–90.

    Google Scholar 

  • Mathie JN, Franklin CE. The influence of body size on the diving behaviour and physiology of the bimodally respiring turtle, Elseya albagula. J Comp Physiol B. 2006;176:739–47.

    Article  PubMed  Google Scholar 

  • Milani A. Beiträge zur Kenntniss der Reptilienlunge. Zool Jahrb. 1894;7:545–92.

    Google Scholar 

  • Milani A. Beiträge zur Kenntnis der Reptilienlunge II. Zool Jahrb. 1897;10:93–156.

    Google Scholar 

  • Miller WS. The structure of the lung. J Morph. 1893;VIII:165–89.

    Article  Google Scholar 

  • Montiero A, Smith RL. Bronchial tree architecture in mammals of diverse body mass. Int J Morphol. 2014;32:312–6.

    Article  Google Scholar 

  • Nysten M. Étude anatomique des rapports de la vessie aérienne avec l’axe vertébral chez Pantodon buchholzi Peters. Ann Mus R l’Afrique Cent Sci Zool. 1962;8:187–220.

    Google Scholar 

  • Perry SF. Reptilian lungs: functional anatomy and evolution. Berlin: Springer; 1983.

    Book  Google Scholar 

  • Perry SF, Duncker HR. Lung architecture, volume and static mechanics in five species of lizards. Respir Physiol. 1978;34:61–81.

    Article  CAS  PubMed  Google Scholar 

  • Perry SF, Schmitz A, Andersen NA, Wallau BR, Nicol S. Descriptive study of the diaphragm and lungs in the short-nosed echidna, Tachyglossus aculeatus (Mammalia: monotremata). J Morphol. 2000;243:247–55.

    Article  CAS  PubMed  Google Scholar 

  • Pick FK. Zur feineren Anatomie der Lunge von Halicore dugong. Archiv für Naturgeschichte. 1907;73:245–72.

    Google Scholar 

  • Sagemehl M. Beitrage zur vergleichenden Anatomie der Fische-III. Das Cranium der Characiniden nebst allgemeinen Bemerkungen uber die mit dem Weber’schen Apparat versehenen Physostomenfamilien. Morphol Jahrb. 1885;1885:1–119.

    Google Scholar 

  • Schachner ER, Cieri RL, Butler JP, Farmer CG. Unidirectional pulmonary airflow patterns in the savannah monitor lizard. Nature. 2014;506:367–70.

    Article  CAS  PubMed  Google Scholar 

  • Schmidt-Neilsen K. How birds breathe. Sci Am. 1971;225:72–9.

    Article  Google Scholar 

  • Van Wallach V. The lungs of snakes. In: Gans C, Gaunt AS, editors. Biology of the Reptilia, Morphology G. Visceral Organs, vol. 19. Ithaca, NY: Society for the Study of Amphibians and Reptiles; 1998. p. 93–295.

    Google Scholar 

  • Weibel ER. Morphometry of the human lung. Berlin: Springer; 1963.

    Book  Google Scholar 

  • Weibel ER. The pathway for oxygen. Cambridge: Harvard University Press; 1984.

    Google Scholar 

  • West JB. Respiratory physiology—the essentials. Baltimor: Williams and Wilkins; 1995.

    Google Scholar 

  • Whitford WG, Hutchison VH. Gas exchange in salamanders. Physiol Zool. 1965;38:228–42.

    Article  Google Scholar 

  • Wolf S. Zur kenntnis von Bau und Funktion der Reptilienlunge. Zool Jahrb Abt Anat Ontol. 1933;57:139–90.

    Google Scholar 

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Acknowledgments

I thank Brent Craven and Robert Cieri for modeling work and advice, and Robert Cieri, Scott Echols, Adam Huttenlocker, Jeremy Klingler, Nicola Nelson, and Brett Gartrell, for help obtaining CT data.

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Authors and Affiliations

  1. Trinity College Dublin, University of Dublin, Dublin 2, Ireland

    C. G. Farmer

  2. Department of Biology, University of Utah, Salt Lake City, UT, USA

    C. G. Farmer

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  1. C. G. Farmer
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Correspondence to C. G. Farmer .

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Editors and Affiliations

  1. Department of Zoology, University of Johannesburg, Johannesburg, South Africa

    John N. Maina

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Farmer, C.G. (2017). Pulmonary Transformations of Vertebrates. In: Maina, J. (eds) The Biology of the Avian Respiratory System. Springer, Cham. https://doi.org/10.1007/978-3-319-44153-5_3

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