Dorsoventral inversion of the air‐filled organ (lungs, gas bladder) in vertebrates: RNAsequencing of laser capture microdissected embryonic tissue

Funk, Emily; Lencer, Ezra; McCune, Amy R.

doi:10.1002/jez.b.22998

Cited by 11 publications

(25 citation statements)

References 59 publications

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“…14, Supplementary Note 7). Additionally, we show that this ncOCR activity correlates with critical timing of tbx4 expression during bow n gas bladder development 26 (Fig. 4E, Supplementary Note 7).…”

Section: Chromatin Pro Ling Through Bow N Development Connects Gene Rmentioning

confidence: 65%

“…Bow n features a unique suite of developmental, immunological, morphological, and behavioral phenotypes 2 ripe for study with genomic sequence information, including, e.g. a derived type of dermal scales 25 , air breathing with a gas bladder 26,27 , and a largely ancestral skeletal con guration 1,15 . Genomic resources for the bow n are thus poised to provide key insights into vertebrate developmental evolution.…”

Section: Introductionmentioning

confidence: 99%

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The genome of the bowfin (Amia calva) illuminates the developmental evolution of ray-finned fishes

Thompson

Hawkins

Parey

et al. 2020

Preprint

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The bowfin fish (Amia calva) diverged before the genome duplication in teleost fishes, and its archetypical body plan and slow rate of molecular evolution make it a key species for genomic exploration as a basal representative of the neopterygian fishes. To investigate the evolution and development of ray-finned fishes, we generated a chromosome-level genome assembly for bowfin that enables gene-order analyses which settle its long-debated, phylogenetic relationship with gars. We analyze the genomic underpinnings of the bowfin’s unique combination of derived and ancestral phenotypes involving the immune system as well as scale, respiratory organ, and skeletal development. By detailing chromatin accessibility and gene expression through bowfin development, we connect developmental gene regulatory loci across vertebrates. We illustrate the utility of these genomic resources to connect developmental evolution across bony fishes, showing the importance of bowfin in understanding vertebrate biology and diversity.

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Section: Chromatin Pro Ling Through Bow N Development Connects Gene Rmentioning

confidence: 65%

Section: Introductionmentioning

confidence: 99%

The genome of the bowfin (Amia calva) illuminates the developmental evolution of ray-finned fishes

Thompson

Hawkins

Parey

et al. 2020

Preprint

Self Cite

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“…Modern developmental genetics may help illuminate the mechanisms underlying these morphological changes. Recent work suggests that genes involved in early lung budding are also involved in early gas bladder budding (Cass et al, 2013; Feiner et al, 2009; Funk, Breen, Sanketi, Kurpios, & McCune, 2020; Funk, Lencer, & McCune, 2020; Winata et al, 2009; Zheng et al, 2011). Coincident with the morphological inversion of budding direction between lungs and the gas bladder, two genes, Tbx5 and Bmp ‐signaling, show expression patterns which are inverted relative to the ventral‐dorsal axis during lung and gas bladder development.…”

Section: Discussionmentioning

confidence: 99%

“…Tbx5 is a transcription factor essential for lung budding and branching in mouse (Arora et al, 2012). During lung development in tetrapods and bichirs, the only ray‐finned fish lineage that possess ventral lungs, Tbx5 is expressed in the ventral mesoderm surrounding the lung buds (Arora et al, 2012; Funk, Lencer, et al, 2020; Tatsumi et al, 2016). In contrast, during gas bladder development in bowfin, Tbx5 is expressed in the dorsal mesoderm surrounding the gas bladder bud, an inverted expression pattern relative to that in lungs (Funk, Lencer, et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

“…During lung development in tetrapods and bichirs, the only ray‐finned fish lineage that possess ventral lungs, Tbx5 is expressed in the ventral mesoderm surrounding the lung buds (Arora et al, 2012; Funk, Lencer, et al, 2020; Tatsumi et al, 2016). In contrast, during gas bladder development in bowfin, Tbx5 is expressed in the dorsal mesoderm surrounding the gas bladder bud, an inverted expression pattern relative to that in lungs (Funk, Lencer, et al, 2020). Tbx5 is part of a network of genes, including Tbx4 , Wnt2 , and Fgf10 , known to interact during lung development (Lü et al, 2005; Ng et al, 2002; Sakiyama et al, 2003), all of which appear to show an inverted expression pattern across the dorsoventral axis of the foregut during gas bladder development in bowfin (Funk, Lencer, et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

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Does the bowfin gas bladder represent an intermediate stage during the lung‐to‐gas bladder evolutionary transition?

Funk

Birol

McCune

2021

Journal of Morphology

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Whether phenotypic evolution occurs gradually through time has prompted the search for intermediate forms between the ancestral and derived states of morphological features, especially when there appears to be a discontinuous origin. The gas bladder, a derived character of the Actinopteri, is a modification of lungs, which characterize the common ancestor of bony vertebrates. While gas bladders and lungs are similar in many ways, the key morphological difference between these organs is the direction of budding from the foregut during development; essentially, the gas bladder buds dorsally and the lungs bud ventrally from the foregut. Did the shift from ventral lungs to dorsal gas bladder transition through a lateral‐budding stage? To answer this question, the precise location of budding during gas bladder development in bowfin, representing the sister lineage to teleosts, has been debated. In the early 20th‐century, it was suggested that the bowfin gas bladder buds laterally from the right wall of the foregut. We used nano‐CT scanning to visualize the early development of the bowfin gas bladder to verify the historical studies of gas bladder developmental morphology and determine whether the direction of gas bladder budding in bowfin could be intermediate between ventrally budding lungs and dorsally budding gas bladders. We found that the bowfin gas bladder buds dorsally from the anterior foregut; however, during early development, the posterior gas bladder twists right. As development progresses, the posterior, right‐hand twist becomes shallower, and the gas bladder itself shifts toward a mid‐dorsal position. The budding site is definitively dorsal, despite the temporary lateral twist of the posterior gas bladder.

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Buoyancy control and air breathing in royal knifefish (Chitala blanci) and a new hypothesis for the early evolution of vertebrate air‐breathing behaviors

Kaczmarek,

Brainerd

2024

The Anatomical Record

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We present the first description of inspiration‐first air breaths in royal knifefish, Chitala blanci, a ray‐finned fish known to use four‐stroke air breaths. Four‐stroke breaths are used by nearly all ray‐finned fish species that use their gas bladder to breathe air and are the ancestral breath type of ray‐finned fishes. Interestingly, one such species, Amia calva, is known to perform two distinct breath types. Amia use four‐stroke breaths when they need more oxygen and performs inspiration‐first breaths to restore buoyancy. We observed that C. blanci also performs inspiration‐first breaths and tested whether the two breath types are performed for the same functions in C. blanci as they are in Amia. We recorded the frequency of each breath type when exposed to aquatic hypoxia and two conditions of oxygen availability. We found that C. blanci performed more four‐stroke breaths (81% ± 15% of total breaths) than inspiration‐first breaths when exposed to aerial normoxia but performed more inspiration‐first breaths (72% ± 40%) than four‐stroke breaths when exposed to aerial hyperoxia. These patterns match those described for Amia and indicate that C. blanci performs four‐stroke breaths in response to oxygen depletion and performs inspiration‐first breaths to maintain buoyancy. Few studies have examined the role of air‐breathing in buoyancy regulation. Decreasing buoyancy, rather than oxygen availability, to stimulate air breaths may reveal that inspiration‐first breaths are more common among fishes than we are aware. We consider this possibility and present a new hypothesis for the origin and early evolution of air breathing in vertebrates.

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Dorsoventral inversion of the air‐filled organ (lungs, gas bladder) in vertebrates: RNAsequencing of laser capture microdissected embryonic tissue

Cited by 11 publications

References 59 publications

The genome of the bowfin (Amia calva) illuminates the developmental evolution of ray-finned fishes

The genome of the bowfin (Amia calva) illuminates the developmental evolution of ray-finned fishes

Does the bowfin gas bladder represent an intermediate stage during the lung‐to‐gas bladder evolutionary transition?

Buoyancy control and air breathing in royal knifefish (Chitala blanci) and a new hypothesis for the early evolution of vertebrate air‐breathing behaviors

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