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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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Related in: MedlinePlus

Development of the appendicular skeleton in N. sahyadrensis.(A) Right side of the pectoral girdle at stage 38. (B) Right side of the pectoral girdle at stage 41. (C) Right side of the pectoral girdle at stage 42. Note the cartilaginous epicoracoid, bridging clavicle and coracoid. (D) Forelimbs attached to the pectoral girdle via proximal end of humeri, stage 45. (E) Manus at stage 46. (F) Lateral view of the pelvis at stage 42. (G) Dorsal view of the pelvis at stage 42. (H) Dorsolateral view of the pelvic girdle at stage 45. (I) Dorsal view of tarsals at stage 45. (J) Dorsal view of hind limb at stage 45. (K) Lateral view of prehallux at stage 45. Abbreviations: AC, acetabulum; CL, clavicle; CP2, carpal 2; CP (3–5), fused carpals 3–5; CR, coracoid; CT, cleithrum; DPP, distal prepollex; EC, epicoracoid cartilage; EY, element Y; FB, fibulare; FM, femur; HU, humerus; IL, ilium; IS, ischium; MC, metacarpals; MT, metatarsals; PC, procoracoid cartilage; PD, phalange digits; PH, prehallux; PH1, distal prehallux 1; PH2, distal prehallux 2; PH3, distal prehallux 3; PP, prepollex; PU, pubis; RD, radiale; RU, radioulna; SP, scapula; SS, suprascapula; TB, tibiale; TF, tibiafibulare; T3, tarsal 3; UL, ulnare. Scale bars: 1 mm.
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pone.0151114.g006: Development of the appendicular skeleton in N. sahyadrensis.(A) Right side of the pectoral girdle at stage 38. (B) Right side of the pectoral girdle at stage 41. (C) Right side of the pectoral girdle at stage 42. Note the cartilaginous epicoracoid, bridging clavicle and coracoid. (D) Forelimbs attached to the pectoral girdle via proximal end of humeri, stage 45. (E) Manus at stage 46. (F) Lateral view of the pelvis at stage 42. (G) Dorsal view of the pelvis at stage 42. (H) Dorsolateral view of the pelvic girdle at stage 45. (I) Dorsal view of tarsals at stage 45. (J) Dorsal view of hind limb at stage 45. (K) Lateral view of prehallux at stage 45. Abbreviations: AC, acetabulum; CL, clavicle; CP2, carpal 2; CP (3–5), fused carpals 3–5; CR, coracoid; CT, cleithrum; DPP, distal prepollex; EC, epicoracoid cartilage; EY, element Y; FB, fibulare; FM, femur; HU, humerus; IL, ilium; IS, ischium; MC, metacarpals; MT, metatarsals; PC, procoracoid cartilage; PD, phalange digits; PH, prehallux; PH1, distal prehallux 1; PH2, distal prehallux 2; PH3, distal prehallux 3; PP, prepollex; PU, pubis; RD, radiale; RU, radioulna; SP, scapula; SS, suprascapula; TB, tibiale; TF, tibiafibulare; T3, tarsal 3; UL, ulnare. Scale bars: 1 mm.

Mentions: Ossification of the appendicular skeleton begins before metamorphic climax. Scapular ossifications extend along the scapular cartilage. The paired cleithra, clavicles and coracoids are beginning to ossify (Fig 6A). The clavicle extends from the medial margin of the suprascapula cartilage along the anterior border of the procoracoid cartilage. The cylindrical coracoid extends from the diaphysis of the epicoracoid cartilage. Developing forelimbs are visible beneath the operculum. Radius and ulna are longer and fused medially. The cartilaginous primordium of the ulnare is visible, but other carpals are not. A single cartilaginous prepollical element is present, adjacent to the second digit. Metacarpals II–V and proximal phalanges of digits III and IV ossify as medial centers along their corresponding cylindrical cartilages. Ilia are longer, but neither the ischium nor the pubis is visible. Most of the long bones within the hind limb are visible. The femur extends along the diaphysis of its cartilaginous primordium. Medial ossifications are visible within the cartilaginous primordia of the remaining long bones of the hind limb—tibiafibulare, tibiale and fibulare. Tibia and fibula are fused medially but free at their proximal and distal ends. Cartilaginous primordia of tarsals and the prehallux are present. Metatarsals and proximal phalanges of digits I–V are ossified medially.


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)

Development of the appendicular skeleton in N. sahyadrensis.(A) Right side of the pectoral girdle at stage 38. (B) Right side of the pectoral girdle at stage 41. (C) Right side of the pectoral girdle at stage 42. Note the cartilaginous epicoracoid, bridging clavicle and coracoid. (D) Forelimbs attached to the pectoral girdle via proximal end of humeri, stage 45. (E) Manus at stage 46. (F) Lateral view of the pelvis at stage 42. (G) Dorsal view of the pelvis at stage 42. (H) Dorsolateral view of the pelvic girdle at stage 45. (I) Dorsal view of tarsals at stage 45. (J) Dorsal view of hind limb at stage 45. (K) Lateral view of prehallux at stage 45. Abbreviations: AC, acetabulum; CL, clavicle; CP2, carpal 2; CP (3–5), fused carpals 3–5; CR, coracoid; CT, cleithrum; DPP, distal prepollex; EC, epicoracoid cartilage; EY, element Y; FB, fibulare; FM, femur; HU, humerus; IL, ilium; IS, ischium; MC, metacarpals; MT, metatarsals; PC, procoracoid cartilage; PD, phalange digits; PH, prehallux; PH1, distal prehallux 1; PH2, distal prehallux 2; PH3, distal prehallux 3; PP, prepollex; PU, pubis; RD, radiale; RU, radioulna; SP, scapula; SS, suprascapula; TB, tibiale; TF, tibiafibulare; T3, tarsal 3; UL, ulnare. Scale bars: 1 mm.
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Related In: Results  -  Collection

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

pone.0151114.g006: Development of the appendicular skeleton in N. sahyadrensis.(A) Right side of the pectoral girdle at stage 38. (B) Right side of the pectoral girdle at stage 41. (C) Right side of the pectoral girdle at stage 42. Note the cartilaginous epicoracoid, bridging clavicle and coracoid. (D) Forelimbs attached to the pectoral girdle via proximal end of humeri, stage 45. (E) Manus at stage 46. (F) Lateral view of the pelvis at stage 42. (G) Dorsal view of the pelvis at stage 42. (H) Dorsolateral view of the pelvic girdle at stage 45. (I) Dorsal view of tarsals at stage 45. (J) Dorsal view of hind limb at stage 45. (K) Lateral view of prehallux at stage 45. Abbreviations: AC, acetabulum; CL, clavicle; CP2, carpal 2; CP (3–5), fused carpals 3–5; CR, coracoid; CT, cleithrum; DPP, distal prepollex; EC, epicoracoid cartilage; EY, element Y; FB, fibulare; FM, femur; HU, humerus; IL, ilium; IS, ischium; MC, metacarpals; MT, metatarsals; PC, procoracoid cartilage; PD, phalange digits; PH, prehallux; PH1, distal prehallux 1; PH2, distal prehallux 2; PH3, distal prehallux 3; PP, prepollex; PU, pubis; RD, radiale; RU, radioulna; SP, scapula; SS, suprascapula; TB, tibiale; TF, tibiafibulare; T3, tarsal 3; UL, ulnare. Scale bars: 1 mm.
Mentions: Ossification of the appendicular skeleton begins before metamorphic climax. Scapular ossifications extend along the scapular cartilage. The paired cleithra, clavicles and coracoids are beginning to ossify (Fig 6A). The clavicle extends from the medial margin of the suprascapula cartilage along the anterior border of the procoracoid cartilage. The cylindrical coracoid extends from the diaphysis of the epicoracoid cartilage. Developing forelimbs are visible beneath the operculum. Radius and ulna are longer and fused medially. The cartilaginous primordium of the ulnare is visible, but other carpals are not. A single cartilaginous prepollical element is present, adjacent to the second digit. Metacarpals II–V and proximal phalanges of digits III and IV ossify as medial centers along their corresponding cylindrical cartilages. Ilia are longer, but neither the ischium nor the pubis is visible. Most of the long bones within the hind limb are visible. The femur extends along the diaphysis of its cartilaginous primordium. Medial ossifications are visible within the cartilaginous primordia of the remaining long bones of the hind limb—tibiafibulare, tibiale and fibulare. Tibia and fibula are fused medially but free at their proximal and distal ends. Cartilaginous primordia of tarsals and the prehallux are present. Metatarsals and proximal phalanges of digits I–V are ossified medially.

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