Studies on amphibian metamorphosis. I. Formation of the opercular leg perforation in anuran larvae during metamorphosis

Helff, O. M.

doi:10.1002/jez.1400450102

Cited by 33 publications

(10 citation statements)

References 7 publications

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“…We noticed that the bipartite stages often showed size asymmetry, with the left side larger than the right. This does not seem to have been noticed before, and it is hard to envisage any functional significance, but it is well known that other features of tadpoles are also asymmetric in many taxa: for example, left-side spiracle position in Orton Type 4 tadpoles and the report that left forelimbs emerge some hours before right forelimbs at metamorphosis (Helff, 1926).…”

Section: Discussionmentioning

confidence: 90%

Larval cement gland of frogs: Comparative development and morphology

Nokhbatolfoghahai

Downie

2005

J. Morphol.

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The cement gland (CG) is a transient mucus-secreting organ, found in most anuran embryos and early larvae and located normally on the anteroventral side of the head. Its sticky secretion allows newly hatched larvae to attach to the egg jelly or to another support and remain hidden and stationary until feeding starts. Analysis of CG morphology in 20 anuran species from six families using scanning electron microscopy revealed five distinct patterns of development, which partly related to families. The five patterns are described, as well as additional details such as CG surface ciliation and asymmetry. Three species lacked a CG. This was expected in two cases, a late-hatching phyllomedusine hylid and a direct-developing eleutherodactylid, but not in the foam-nesting Leptodactylus fuscus, which hatches at the same stage as many species that develop a CG. Lack of the CG in L. fuscus suggests that its posthatching period in the foam nest may be obligate. In both L. fuscus and the phyllomedusine hylid, there remain morphological traces of CG development.

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Section: Discussionmentioning

confidence: 90%

Larval cement gland of frogs: Comparative development and morphology

Nokhbatolfoghahai

Downie

2005

J. Morphol.

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“…T 3 treatment rescued these suturing events (Fig. 3F), which have an intriguing parallel in biphasic frogs, where ventral suturing occurs in the corresponding region after the limbs burst through the operculum during metamorphic climax (25,26).…”

Section: Establishment Of Assay Conditionsmentioning

confidence: 81%

Thyroid hormone-dependent metamorphosis in a direct developing frog

Callery

Elinson

2000

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

111

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The direct developing anuran, Eleutherodactylus coqui, lacks a tadpole, hatching as a tiny frog. We investigated the role of the metamorphic trigger, thyroid hormone (TH), in this unusual ontogeny. Expression patterns of the thyroid hormone receptors, TR␣ and TR␤, were similar to those of indirect developers. TR␤ mRNA levels increased dramatically around the time of thyroid maturation, when remodeling events reminiscent of metamorphosis occur. Treatment with the goitrogen methimazole inhibited this remodeling, which was reinitiated on cotreatment with TH. Despite their radically altered ontogeny, direct developers still undergo a TH-dependent metamorphosis, which occurs before hatching. We propose a new model for the evolution of anuran direct development.T he term ''amphibian'' conveys the image of a dual life history, split between water and land. However, 29 different anuran reproductive modes have been defined, on the basis of the site of egg development (1). Included in this developmental smorgasbord are species in which the larvae develop inside a foam nest (Chiromantis), those that brood live embryos in their stomach (Rheobatrachus), ''marsupial frogs'' in which the tadpoles develop within a parental pouch (Gastrotheca), and the most extreme modification, direct development, where the freeliving larva has been deleted from the life history (Eleutherodactylus).Direct development in Eleutherodactylus is a derived characteristic (2), yet embryogenesis in these frogs is so radically modified that little hint of their biphasic metamorphic ancestry is visible. Development is entirely terrestrial, with tiny froglets hatching from their jelly capsules 3 wk after fertilization. Many larval characteristics are lacking, including cement gland, lateral line organs, coiled gut, larval mouth parts, and some cranial cartilages (3). The only obviously larval feature is the tail, which shrinks before hatching.The ontogenetic modifications responsible for direct development are unknown. Because direct developers are thought to have evolved from biphasic frogs (1, 2), the role of thyroid hormone (TH) in direct development is of particular interest. TH, shown in other systems to signal through thyroid hormone receptors (TRs), controls the larval-to-adult transition in biphasic frogs (4). TR␤ expression in both Xenopus laevis and Rana catesbeiana is temporally correlated with the onset of metamorphosis, implicating this gene as a likely metamorphic mediator (5-7). The role of TH in direct development is unclear. Both chemical and surgical ablation of the thyroid axis in Eleutherodactylus martinicensis inhibited tail regression and pronephric degeneration (8, 9). These events were precociously induced by 3,3Ј,5-triiodothyronine (T 3 ) treatment, but other organ systems appeared unaffected (8). Although the similarity between such degenerative changes in Eleutherodactylus and those occurring in metamorphosis was noted, the specificity of effects caused by drug treatment was questioned. It was thought likely by these authors tha...

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“…Yet up to 90-100% of all individuals in a given population show first emergence of the forelimb on the same side. Moreover, it was repeatedly shown that forelimbs are unlikely to influence mechanically the perforation of the opercular folds in directly developing Eleutherodactylus and possessing tadpole stage Rana (Callery & Elinson, 2000;Helff, 1926;Sasaki, Takahama, Horiguchi, & Watanabe, 1983) as the perforation is formed even after one-sided forelimb ablation. However, the possibility of an influence of forelimb use preference on the order of forelimb emergence may still exist.…”

Section: Forelimb Emergence In Tadpoles and Forelimb Use In Adultsmentioning

confidence: 98%

Asymmetries in amphibians: A review of morphology and behaviour

Malashichev

2002

Laterality: Asymmetries of Body, Brain and Cognition

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Morphological and behavioural asymmetries in amphibians are reviewed. Among the characteristics considered are: (1) the asymmetry of the shoulder girdle (epicoracoid overlap); (2) the distribution of the left and right variants of its structure in amphibian populations; (3) asymmetry in the position of the spiracle(s); (4) asymmetric order of forelimb emergence from opercular chambers in tadpoles; and (5) preferential forelimb use in adult amphibians. I show that there are no direct cause-and-effect relationships between these characteristics, which would explain their development. Other asymmetries, such as asymmetry of the visceral organs, turning behaviour of tadpoles, asymmetries in the length and weights of the long bones, and some neuromorphological traits, also show few examples of relationships. However, the simultaneous absence of many asymmetries in some amphibians and their presence in others suggests a common cause, which affects all of these asymmetries indirectly, presumably very early in ontogenesis.

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Studies on amphibian metamorphosis. I. Formation of the opercular leg perforation in anuran larvae during metamorphosis

Cited by 33 publications

References 7 publications

Larval cement gland of frogs: Comparative development and morphology

Larval cement gland of frogs: Comparative development and morphology

Thyroid hormone-dependent metamorphosis in a direct developing frog

Asymmetries in amphibians: A review of morphology and behaviour

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