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From Clinging to Digging: The Postembryonic Skeletal Ontogeny of the Indian Purple Frog, Nasikabatrachus sahyadrensis (Anura: Nasikabatrachidae).

Senevirathne G, Thomas A, Kerney R, Hanken J, Biju SD, Meegaskumbura M - PLoS ONE (2016)

Bottom Line: The subsequent ontogenetic shift from clinging to digging is correlated with rapid morphological changes and behavioral modifications.Metamorphs are equipped with a shortened tibiafibula and ossified prehallical elements, which likely facilitate initial digging using the hind limbs.Subsequently, the frogs may shift to headfirst burrowing by using the wedge-shaped skull, anteriorly positioned pectoral girdle, well-developed humeral crests and spatula-shaped forelimbs.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology & Biotechnology, Faculty of Science, University of Peradeniya, Peradeniya, Sri Lanka.

ABSTRACT
The Indian Purple frog, Nasikabatrachus sahyadrensis, occupies a basal phylogenetic position among neobatrachian anurans and has a very unusual life history. Tadpoles have a large ventral oral sucker, which they use to cling to rocks in torrents, whereas metamorphs possess adaptations for life underground. The developmental changes that underlie these shifts in habits and habitats, and especially the internal remodeling of the cranial and postcranial skeleton, are unknown. Using a nearly complete metamorphic series from free-living larva to metamorph, we describe the postembryonic skeletal ontogeny of this ancient and unique monotypic lineage. The torrent-dwelling larva possesses a dorsoventrally flattened body and a head with tiny dorsal eyes, robust lower and upper jaw cartilages, well-developed trabecular horns, and a definable gap between the trabecular horns and the tip of the snout. Unlike tadpoles of many other frogs, those of Nasikabatrachus retain larval mouthparts into late metamorphic stages. This unusual feature enables the larvae to maintain their clinging habit until near the end of metamorphosis. The subsequent ontogenetic shift from clinging to digging is correlated with rapid morphological changes and behavioral modifications. Metamorphs are equipped with a shortened tibiafibula and ossified prehallical elements, which likely facilitate initial digging using the hind limbs. Subsequently, the frogs may shift to headfirst burrowing by using the wedge-shaped skull, anteriorly positioned pectoral girdle, well-developed humeral crests and spatula-shaped forelimbs. The transition from an aquatic life in torrents to a terrestrial life underground entails dramatic changes in skeletal morphology and function that represent an extreme in metamorphic remodeling. Our analysis enhances the scope for detailed comparative studies across anurans, a group renowned for the diversity of its life history strategies.

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Alcian blue-stained neurocranium and the first visceral arch of Nasikabatrachus sahyadrensis at stage 30.(A) Dorsal view. (B) Ventral view. (C) Upper jaw. (D) Lower jaw. Abbreviations: ADS, adrostral cartilage; AP, ascending process; ARP, articular process; ASO, arcus subocularis; COI, commissura intramandibularis; CPF, craniopalatine foramen; IC, infrarostral cartilage; LON, lamina orbitonasalis; LP, lateral process; MC, Meckel’s cartilage; MP, muscular process; NS, nasal septum; NT, nasal tectum; OC, otic capsule; OP, otic process; PCF, primary carotid foramen; QC, quadratocranial commissure; RP, retroarticular process; SA, suprarostral ala; SC, suprarostral cartilage; SF, subocular fenestra; SMC, suprarostral medial corpus; TH, trabecular horns; TS, synotic tectum; TTM, taenia tecti marginalis. Scale bars: 1 mm.
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pone.0151114.g001: Alcian blue-stained neurocranium and the first visceral arch of Nasikabatrachus sahyadrensis at stage 30.(A) Dorsal view. (B) Ventral view. (C) Upper jaw. (D) Lower jaw. Abbreviations: ADS, adrostral cartilage; AP, ascending process; ARP, articular process; ASO, arcus subocularis; COI, commissura intramandibularis; CPF, craniopalatine foramen; IC, infrarostral cartilage; LON, lamina orbitonasalis; LP, lateral process; MC, Meckel’s cartilage; MP, muscular process; NS, nasal septum; NT, nasal tectum; OC, otic capsule; OP, otic process; PCF, primary carotid foramen; QC, quadratocranial commissure; RP, retroarticular process; SA, suprarostral ala; SC, suprarostral cartilage; SF, subocular fenestra; SMC, suprarostral medial corpus; TH, trabecular horns; TS, synotic tectum; TTM, taenia tecti marginalis. Scale bars: 1 mm.

Mentions: Description of the larval neurocranium is based on four stage-30 tadpoles (Fig 1A–1D). The average width of the cranium equals 99% of its length (N = 4); the greatest width is attained at the level of the muscular processes. Trabecular horns extend from the ethmoid plate and are relatively long—46% of chondrocranial length (Fig 1A). The horns are uniform in width but diverge anteriorly, resulting in a V-shape with an angle of 74° with the ethmoid plate. A lateral process arises from the lateral margin of each trabecular horn near its base. Anteriorly, each trabecular horn curves to articulate with lateral alae and central corpus of the suprarostral (upper jaw) cartilage on the same side.


From Clinging to Digging: The Postembryonic Skeletal Ontogeny of the Indian Purple Frog, Nasikabatrachus sahyadrensis (Anura: Nasikabatrachidae).

Senevirathne G, Thomas A, Kerney R, Hanken J, Biju SD, Meegaskumbura M - PLoS ONE (2016)

Alcian blue-stained neurocranium and the first visceral arch of Nasikabatrachus sahyadrensis at stage 30.(A) Dorsal view. (B) Ventral view. (C) Upper jaw. (D) Lower jaw. Abbreviations: ADS, adrostral cartilage; AP, ascending process; ARP, articular process; ASO, arcus subocularis; COI, commissura intramandibularis; CPF, craniopalatine foramen; IC, infrarostral cartilage; LON, lamina orbitonasalis; LP, lateral process; MC, Meckel’s cartilage; MP, muscular process; NS, nasal septum; NT, nasal tectum; OC, otic capsule; OP, otic process; PCF, primary carotid foramen; QC, quadratocranial commissure; RP, retroarticular process; SA, suprarostral ala; SC, suprarostral cartilage; SF, subocular fenestra; SMC, suprarostral medial corpus; TH, trabecular horns; TS, synotic tectum; TTM, taenia tecti marginalis. Scale bars: 1 mm.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4814056&req=5

pone.0151114.g001: Alcian blue-stained neurocranium and the first visceral arch of Nasikabatrachus sahyadrensis at stage 30.(A) Dorsal view. (B) Ventral view. (C) Upper jaw. (D) Lower jaw. Abbreviations: ADS, adrostral cartilage; AP, ascending process; ARP, articular process; ASO, arcus subocularis; COI, commissura intramandibularis; CPF, craniopalatine foramen; IC, infrarostral cartilage; LON, lamina orbitonasalis; LP, lateral process; MC, Meckel’s cartilage; MP, muscular process; NS, nasal septum; NT, nasal tectum; OC, otic capsule; OP, otic process; PCF, primary carotid foramen; QC, quadratocranial commissure; RP, retroarticular process; SA, suprarostral ala; SC, suprarostral cartilage; SF, subocular fenestra; SMC, suprarostral medial corpus; TH, trabecular horns; TS, synotic tectum; TTM, taenia tecti marginalis. Scale bars: 1 mm.
Mentions: Description of the larval neurocranium is based on four stage-30 tadpoles (Fig 1A–1D). The average width of the cranium equals 99% of its length (N = 4); the greatest width is attained at the level of the muscular processes. Trabecular horns extend from the ethmoid plate and are relatively long—46% of chondrocranial length (Fig 1A). The horns are uniform in width but diverge anteriorly, resulting in a V-shape with an angle of 74° with the ethmoid plate. A lateral process arises from the lateral margin of each trabecular horn near its base. Anteriorly, each trabecular horn curves to articulate with lateral alae and central corpus of the suprarostral (upper jaw) cartilage on the same side.

Bottom Line: The subsequent ontogenetic shift from clinging to digging is correlated with rapid morphological changes and behavioral modifications.Metamorphs are equipped with a shortened tibiafibula and ossified prehallical elements, which likely facilitate initial digging using the hind limbs.Subsequently, the frogs may shift to headfirst burrowing by using the wedge-shaped skull, anteriorly positioned pectoral girdle, well-developed humeral crests and spatula-shaped forelimbs.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology & Biotechnology, Faculty of Science, University of Peradeniya, Peradeniya, Sri Lanka.

ABSTRACT
The Indian Purple frog, Nasikabatrachus sahyadrensis, occupies a basal phylogenetic position among neobatrachian anurans and has a very unusual life history. Tadpoles have a large ventral oral sucker, which they use to cling to rocks in torrents, whereas metamorphs possess adaptations for life underground. The developmental changes that underlie these shifts in habits and habitats, and especially the internal remodeling of the cranial and postcranial skeleton, are unknown. Using a nearly complete metamorphic series from free-living larva to metamorph, we describe the postembryonic skeletal ontogeny of this ancient and unique monotypic lineage. The torrent-dwelling larva possesses a dorsoventrally flattened body and a head with tiny dorsal eyes, robust lower and upper jaw cartilages, well-developed trabecular horns, and a definable gap between the trabecular horns and the tip of the snout. Unlike tadpoles of many other frogs, those of Nasikabatrachus retain larval mouthparts into late metamorphic stages. This unusual feature enables the larvae to maintain their clinging habit until near the end of metamorphosis. The subsequent ontogenetic shift from clinging to digging is correlated with rapid morphological changes and behavioral modifications. Metamorphs are equipped with a shortened tibiafibula and ossified prehallical elements, which likely facilitate initial digging using the hind limbs. Subsequently, the frogs may shift to headfirst burrowing by using the wedge-shaped skull, anteriorly positioned pectoral girdle, well-developed humeral crests and spatula-shaped forelimbs. The transition from an aquatic life in torrents to a terrestrial life underground entails dramatic changes in skeletal morphology and function that represent an extreme in metamorphic remodeling. Our analysis enhances the scope for detailed comparative studies across anurans, a group renowned for the diversity of its life history strategies.

Show MeSH
Related in: MedlinePlus