Lung evolution in vertebrates and the water-to-land transition

Author:

Cupello Camila1ORCID,Hirasawa Tatsuya2ORCID,Tatsumi Norifumi3ORCID,Yabumoto Yoshitaka4ORCID,Gueriau Pierre56ORCID,Isogai Sumio7,Matsumoto Ryoko8ORCID,Saruwatari Toshiro910ORCID,King Andrew11ORCID,Hoshino Masato12ORCID,Uesugi Kentaro12ORCID,Okabe Masataka3ORCID,Brito Paulo M1ORCID

Affiliation:

1. Departamento de Zoologia-IBRAG, Universidade do Estado do Rio de Janeiro

2. Department of Earth and Planetary Science, Graduate School of Science, The University of Tokyo

3. Department of Anatomy, The Jikei University School of Medicine

4. Kitakyushu Museum of Natural History and Human History, 2-4-1 Higashida, Yahatahigashi-ku, Kitakyushu

5. Institute of Earth Sciences, University of Lausanne

6. Université Paris-Saclay, CNRS, ministère de la Culture, UVSQ, MNHN, Institut photonique d’analyse non-destructive européen des matériaux anciens

7. Department of Anatomy, Iwate Medical University School of Medicine

8. Kanagawa Prefectural Museum of Natural History

9. Atmosphere and Ocean Research Institute, The University of Tokyo

10. Seikei Education and Research Center for Sustainable Development

11. Synchrotron SOLEIL, L’orme des Merisiers Saint-Aubin

12. Japan Synchrotron Radiation Research Institute (JASRI/SPring-8)

Abstract

A crucial evolutionary change in vertebrate history was the Palaeozoic (Devonian 419–359 million years ago) water-to-land transition, allowed by key morphological and physiological modifications including the acquisition of lungs. Nonetheless, the origin and early evolution of vertebrate lungs remain highly controversial, particularly whether the ancestral state was paired or unpaired. Due to the rarity of fossil soft tissue preservation, lung evolution can only be traced based on the extant phylogenetic bracket. Here we investigate, for the first time, lung morphology in extensive developmental series of key living lunged osteichthyans using synchrotron x-ray microtomography and histology. Our results shed light on the primitive state of vertebrate lungs as unpaired, evolving to be truly paired in the lineage towards the tetrapods. The water-to-land transition confronted profound physiological challenges and paired lungs were decisive for increasing the surface area and the pulmonary compliance and volume, especially during the air-breathing on land.

Funder

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior

Programa de Apoio à Docência

Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro

Interdisciplinary Collaborative Research Program of the Atmosphere and Ocean Research Institute, the University of Tokyo

Prociência Fellowship CNPq

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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