Fins into limbs: Recent insights from sarcopterygian fish

Amaral, Danielson B.; Schneider, Igor

doi:10.1002/dvg.23052

Cited by 20 publications

(28 citation statements)

References 55 publications

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“…Recently, transcriptome analysis revealed strong similarities between the transcriptional profiles deployed in lungfish fin and salamander limb blastemas (LBs) (6). Altogether, current data support the hypothesis that tetrapods inherited a limb regeneration program from sarcopterygian fish ancestors (10).…”

supporting

confidence: 70%

Deep evolutionary origin of limb and fin regeneration

Darnet

Dragalzew

Amaral

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Salamanders and lungfishes are the only sarcopterygians (lobe-finned vertebrates) capable of paired appendage regeneration, regardless of the amputation level. Among actinopterygians (ray-finned fishes), regeneration after amputation at the fin endoskeleton has only been demonstrated in polypterid fishes (Cladistia). Whether this ability evolved independently in sarcopterygians and actinopterygians or has a common origin remains unknown. Here we combine fin regeneration assays and comparative RNA-sequencing (RNA-seq) analysis of Polypterus and axolotl blastemas to provide support for a common origin of paired appendage regeneration in Osteichthyes (bony vertebrates). We show that, in addition to polypterids, regeneration after fin endoskeleton amputation occurs in extant representatives of 2 other nonteleost actinopterygians: the American paddlefish (Chondrostei) and the spotted gar (Holostei). Furthermore, we assessed regeneration in 4 teleost species and show that, with the exception of the blue gourami (Anabantidae), 3 species were capable of regenerating fins after endoskeleton amputation: the white convict and the oscar (Cichlidae), and the goldfish (Cyprinidae). Our comparative RNA-seq analysis of regenerating blastemas of axolotl and Polypterus reveals the activation of common genetic pathways and expression profiles, consistent with a shared genetic program of appendage regeneration. Comparison of RNA-seq data from early Polypterus blastema to single-cell RNA-seq data from axolotl limb bud and limb regeneration stages shows that Polypterus and axolotl share a regeneration-specific genetic program. Collectively, our findings support a deep evolutionary origin of paired appendage regeneration in Osteichthyes and provide an evolutionary framework for studies on the genetic basis of appendage regeneration.

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supporting

confidence: 70%

Deep evolutionary origin of limb and fin regeneration

Darnet

Dragalzew

Amaral

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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“…Recently, a transcriptome analysis revealed strong similarities between the transcriptional profiles deployed in lungfish fin and salamander limb blastemas 6 . Altogether, current data support the hypothesis that tetrapods inherited a limb regeneration program from sarcopterygian fish ancestors 10 .…”

supporting

confidence: 83%

Deep evolutionary origin of limb and fin regeneration

Darnet

Dragalzew

Amaral

et al. 2018

Preprint

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Salamanders and lungfishes are the only sarcopterygians (lobe-finned vertebrates) capable of complete limb and paired fin regeneration, respectively. Among actinopterygians (ray-finned fishes), regeneration after amputation at the fin endoskeleton has only been demonstrated in Polypterid fishes (Cladistia). Whether complete appendage regeneration in sarcopterygians and actinopterygians evolved independently or has a common origin remains unknown. Here we combine fin regeneration assays and comparative RNA-seq analysis to provide support for a common origin of a paired appendage regeneration in osteichthyes (bony vertebrates).We show that, in addition to Polypterids, regeneration after fin endoskeleton amputation occurs in extant representatives of all major actinopterygian clades: the American paddlefish, (Chondrostei), the spotted gar (Holostei), as well as in two cichlid species, the white convict and the oscar (Teleostei). Our comparative RNA-seq analysis of regenerating blastemas of axolotl and Polypterus reveals the activation of common genetic pathways and expression profiles, consistent with a pan-osteichthyes genetic program of appendage regeneration.Collectively, our findings support a deep evolutionary origin of paired appendage regeneration in osteichthyes and provide an evolutionary framework for studies on the genetic basis of appendage regeneration. Δ ΔCT method. methods 25, 402-408 (2001).

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“…Consequently, a detailed anatomical description of the morphology and anatomy of the pectoral fin and girdle at different ontogenetic stages of the extant coelacanth is crucial for an understanding of the development of the pectoral fin of Latimeria in comparison with fossil coelacanths and tetrapodomorphs. The development of the endoskeleton of the pectoral fin and girdle in Latimeria is likely to be informative for reconstructing the plesiomorphic configuration of the pectoral appendages in sarcopterygians (Coates et al, ; Amaral & Schneider, ). Here, we study the development of the pectoral fin and girdle in the extant coelacanth by describing this anatomical complex in a unique ontogenetic series of five stages comprised of three prenatal stages and two post‐natal stages (Dutel et al, ).…”

Section: Introductionmentioning

confidence: 99%

Development and growth of the pectoral girdle and fin skeleton in the extant coelacanthLatimeria chalumnae

Mansuit

Clément²,

Herrel

et al. 2019

Journal of Anatomy

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The monobasal pectoral fins of living coelacanths and lungfishes are homologous to the forelimbs of tetrapods and are thus critical to investigate the origin thereof. However, it remains unclear whether the similarity in the asymmetrical endoskeletal arrangement of the pectoral fins of coelacanths reflects the evolution of the pectoral appendages in sarcopterygians. Here, we describe for the first time the development of the pectoral fin and shoulder girdle in the extant coelacanth Latimeria chalumnae, based on the tomographic acquisition of a growth series. The pectoral girdle and pectoral fin endoskeleton are formed early in development with a radially outward growth of the endoskeletal elements. The visualization of the pectoral girdle during development shows a reorientation of the girdle between the fetus and pup 1 stages, creating a contact between the scapulocoracoids and the clavicles in the ventro‐medial region. Moreover, we observed a splitting of the pre‐ and post‐axial cartilaginous plates in respectively pre‐axial radials and accessory elements on one hand, and in post‐axial accessory elements on the other hand. However, the mechanisms involved in the splitting of the cartilaginous plates appear different from those involved in the formation of radials in actinopterygians. Our results show a proportional reduction of the proximal pre‐axial radial of the fin, rendering the external morphology of the fin more lobe‐shaped, and a spatial reorganization of elements resulting from the fragmentation of the two cartilaginous plates. Latimeria development hence supports previous interpretations of the asymmetrical pectoral fin skeleton as being plesiomorphic for coelacanths and sarcopterygians.

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Fins into limbs: Recent insights from sarcopterygian fish

Cited by 20 publications

References 55 publications

Deep evolutionary origin of limb and fin regeneration

Deep evolutionary origin of limb and fin regeneration

Deep evolutionary origin of limb and fin regeneration

Development and growth of the pectoral girdle and fin skeleton in the extant coelacanthLatimeria chalumnae

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