Lung evolution in vertebrates and the water-to-land transition
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Evaluation Summary:
This study used valuable materials from five osteichthyan vertebrate species and investigated their lung morphology in them. The comparison of the observations suggest an origin of the lung as an unpaired organ, with the present-day paired forms in amniotes being a result of secondary modification. The sound morphological comparison presented provides valuable insight into the evolution of the lung. The work will be of interest to colleagues studying vertebrate evolution.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 and Reviewer #3 agreed to share their name with the authors.)
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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.
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Evaluation Summary:
This study used valuable materials from five osteichthyan vertebrate species and investigated their lung morphology in them. The comparison of the observations suggest an origin of the lung as an unpaired organ, with the present-day paired forms in amniotes being a result of secondary modification. The sound morphological comparison presented provides valuable insight into the evolution of the lung. The work will be of interest to colleagues studying vertebrate evolution.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 and Reviewer #3 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
The authors of this manuscript analyzed the lung morphology of five osteichthyan vertebrate species (four that do not belong to amniotes or teleost fishes plus a salamander) and based on their phylogenetic relationship, they concluded that the lung first arose as an unpaired organ and later became bilaterally paired in the amniote lineage and secondarily lost in the teleost fish lineage. I found the authors' anatomical investigation of morphology enabled by sample collection covering the long-missing osteichthyan lineages appealing and sufficient to draw the conclusion.
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Reviewer #2 (Public Review):
This is an interesting paper that gives novel insights into the evolution of lungs. The study is straightforward. It is well written and the data are clear. The authors have analysed lung development in a number of species of bony fish, which have been chosen as they occupy an informative position on the evolutionary tree. They use synchrotron X-ray microtomography and histology to probe lung development. They conclude that the primitive state of vertebrate lungs was as unpaired structures but with the evolution of land-dwelling vertebrates, truly paired lungs emerged. These are a defining feature of the tetrapods and are crucial for life on land. The authors present a scenario for how they believe lungs evolved which is believable and insightful.
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Reviewer #3 (Public Review):
This paper presents significant new data on the anatomy and developmental biology and evolution of lungs in key basal, key osteichthyan fishes, and a primitive tetrapod. The paper provides a good background to the problem, but one main point that should be considered is missing (see below). The 3D CT data combined with thin-section images substantiate their findings well. The work holds important implications for understanding how paired lungs first evolved in fishes and tetrapods, which has been a major evolutionary conundrum up to now. The methods and data presented are sound, and the illustrations are clear and relevant to the development of the intellectual arguments presented in the discussion.
There is a controversial old description of paired lungs in the placoderm (basal gnathostome) Bothriolepis …
Reviewer #3 (Public Review):
This paper presents significant new data on the anatomy and developmental biology and evolution of lungs in key basal, key osteichthyan fishes, and a primitive tetrapod. The paper provides a good background to the problem, but one main point that should be considered is missing (see below). The 3D CT data combined with thin-section images substantiate their findings well. The work holds important implications for understanding how paired lungs first evolved in fishes and tetrapods, which has been a major evolutionary conundrum up to now. The methods and data presented are sound, and the illustrations are clear and relevant to the development of the intellectual arguments presented in the discussion.
There is a controversial old description of paired lungs in the placoderm (basal gnathostome) Bothriolepis (Denison 1941; Arsenault et al 2004; Goujet 2011, Janvier et a.l 2007) which is completely contrary to the main conclusions of this paper. One cannot simply ignore it - the authors must confront the data and discuss it, or else there is standing evidence that the basal condition for all gnathostomes is a paired lung.
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