Direct-developing frogs: ontogeny of Oreobates barituensis (Anura: Terrarana) and the development of a novel trait

in Amphibia-Reptilia
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Within Anura, direct development involves ontogenetic changes of the biphasic ancestral pattern. The recent partitioning of the genus Eleutherodactylus, along with the proposition of the unranked taxon Terrarana, has renewed an interest to the morphological and ecological diversity among direct-developing frogs. The morphological changes during embryonic development of Oreobates barituensis is similar to those of other Neotropical direct-developing species, including the reduction or absence of several larval and embryonic characters (e.g., external gills and adhesive glands), heterochronic changes (e.g., early developing limbs and late persistence of ciliated epidermal cells), and the appearance of new structures (e.g., egg tooth). The tail achieves an extraordinary peramorphic development (encloses the entire embryo), and the location of its expanded part is interpreted as a heterotopic change resulting in a novel trait. An enveloping tail with apparently non-heterotopic fins, combined with the absence of gills, has been only reported for a species of the related genus Craugastor, and these morphologies suggest an informative perspective for the study of evolution of direct development in terraranans.

Direct-developing frogs: ontogeny of Oreobates barituensis (Anura: Terrarana) and the development of a novel trait

in Amphibia-Reptilia



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    External development in pre-hatching stages of Oreobates barituensis. Jelly layers have been removed and contrast was increased with methylene blue. Stages of Townsend and Stewart (1985; TS) are indicated. (A) TS4, dorsal view. Note bulges of the gill arches and forelimbs. (B) TS5, dorsal, anterolateral, and rear views. Note the dermal fold at the base of the forelimb, and the lateral extensions of the tail. (C) TS6, dorsal view. The lateral extensions of the tail surround the embryo completely. Pictures within the square are details of the anterior and posterior parts once the tail extensions have been removed. (D) TS10-11, dorsal and posteroventral views. Note the highly vascularized tail extension with a small gap. (E) TS12-13, lateral view. Note the small gap in the tail extensions. (F) Same specimens as in D, with the tail extensions removed. Note the egg tooth and the dermal fold. (G) Same specimen as in E, with the tail extensions removed. Note the keratinized egg tooth. (H) TS13, ventral and lateral views, showing the tail regressing. (I) TS14-15, dorsal and lateral views, showing more advanced tail regression. DF: dermal fold; ET: egg tooth; FL: forelimb; G: gap in the enveloping tail; GA: gill arches; TE: tail extension; VT: vent tube. Scale bars = 1 mm.

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    Post-hatching specimens of Oreobates barituensis. (A) Specimen with a vestige of the tail. (B) Specimen with the tail completely resorbed. Scale bars = 1 mm.

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    Tail cross sections. (A) Scinax acuminatus pond tadpole. (B) Oreobates barituensis, tail distal portion with a detail of large blood vessels in the lateral extensions. The spinal cord/notochord axis is in line with the fins in (A) but perpendicular to the lateral extensions in (B); also note the large blood vessels in contact with the epidermis in Oreobates. BV: blood vessel; DF: dorsal fin; M: muscles; N: notochord; S: spinal cord; T: tail extension; VF: ventral fin. Scale bars = 1 mm (A) and 0.1 mm (B). This figure is published in colour in the online version.

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    Scanning electron micrographs of specimens of Oreobates barituensis. (A) TS6, ciliated cells from yolk mass (left, as indicated by the asterisk) and detail of the ciliated hind limbs and vent tube (right). (B) TS12, ciliated cells from the nostril region (left, as indicated by the asterisk) and detail of the egg tooth (right).

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    Plots comparing embryonic development of Eleutherodactylus coqui (dotted lines) and Oreobates barituensis (solid lines). (A) Rates of time development per stage of Townsend and Stewart (1985). Timing in E. coqui was taken from the original paper, and an average of the described developmental period (17-26 days) was used. Embryos were raised at comparable temperatures (20-25°C). Note that embryonic development in O. barituensis takes longer mainly because of an arrested rate at later stages. (B) Limbs and tail developmental events. The Y-axis represents shape stages in limb and tail development, described in two separate ordinal scales. Limb development is defined as the sequential differentiation of limb buds, elbows and knees, and toes, and finally toe elongation; note the similar onset and the isomorphic limb final shape achieved after a slower rate and a later offset in O. barituensis. Tail development is summarized as tail bud stage, full tail 70% the snout-vent length, and full enveloping tail; in O. barituensis, a peramorphic final shape results from an accelerated rate.

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