A Tale of a Tail: Variation during the Early Ontogeny of Haddadus binotatus (Brachycephaloidea: Craugastoridae) as Compared with Other Direct Developers
The New World direct-developing frogs (Brachycephaloidea = Terrarana) comprise nearly a thousand species that share direct development among other putative synapomorphies, yet embryonic development in this group has been thoroughly described in only about 20 species. Here we describe the early ontogeny of the craugastorid Haddadus binotatus, making special emphasis on tail structure and development, and its differences and similarities with that of other terraranans. The morphological changes during embryonic development of H. binotatus and those of other Neotropical direct-developing species are alike, with some variation including the absence of external gills, timing of limb differentiation, and tail configuration. The tail with a rotated core axis and lateral and asymmetric fins that cover the posterior half of the embryo represents an outstanding case of developmental repatterning. We present some interpretations of the evolution of the tail and its three major aspects, the rotation of the core axis, and the origin and extensions of the fins, and pinpoint that those mechanisms underlying fin development should be fairly plastic, allowing the ontogenetic and evolutionary variation within the Brachycephaloidea clade. Las ranas de desarrollo directo del Nuevo Mundo (Brachycephaloidea = Terrarana) incluyen cerca de mil especies que comparten el desarrollo directo entre otras sinapomorfías putativas; sin embargo el desarrollo embrionario en este grupo ha sido descripto en no más de 20 especies. Aquí describimos la ontogenia temprana del craugastórido Haddadus binotatus, con especial énfasis en la estructura y el desarrollo de la cola y sus diferencias y similitudes con la de otros terraranas. Los cambios morfológicos durante el desarrollo embrionario de H. binotatus son similares a los de otras ranas neotropicales con desarrollo directo, con algunas variaciones que incluyen la ausencia de branquias externas, los tiempos de diferenciación de las extremidades y la configuración de la cola. La cola con su eje rotado y aletas laterales y asimétricas que cubren la mitad posterior del embrión representa un caso excepcional de cambio en los patrones del desarrollo. Aquí presentamos algunas interpretaciones sobre la evolución de la cola y sus tres aspectos principales: la rotación del eje y el origen y extensión de las aletas, y señalamos que los mecanismos que subyacen al desarrollo de la aleta parecen ser lo suficientemente plásticos como para permitir la variación ontogenética y evolutiva presente en el clado Brachycephaloidea.Abstract
Resumen
Developmental series of Haddadus binotatus, from Townsend & Stewart stage 6–7 to hatching. The vitellum was removed in the two first specimens to photograph the hind limbs (insets with arrows), covered by the sac-like tail. Note the limb size difference at TS8. The dermal fold is indicated with an asterisk (*). Scale lines = 1 mm.
Details of the tail, dorsal view. Note the origin of the left fin (arows), slightly more rostral than the right fin, especially evident at TS12 and 14. Scale lines = 0.5 mm.
Transverse section through the tail at TS6–7 and detail of the tail fin. Disregarding the odd, disaggregated appearance of the tail tissue (a fixation artifact), note the axis rotation, the pattern of fin disposition, and the fins formed of numerous epithelial folds that likely increase gas exchanging surface. ebv, empty blood vessel; ec, epithelial cell; f, fibroblast; fbv, full blood vessel; m, muscle anlagen; nc, notochord; nt, neural tube. Scale lines = 0.5 mm and 0.05 mm (inset).
Transverse sections through the tail from the base (left) to the tip (right) at TS12, showing the rotated axis and the origin of the fins. Note the base with a slightly rotated axis and fins originating dorsolaterally at the same level, and the right fin originating more ventrolaterally as the tail axis rotates toward the tip. The arrow points out the portion of the tail fin folding on itself; note also the lamellar-like epithelium in that region (inset). Scale lines = 0.3 mm and 0.1 mm (inset).
Histological sections at the base of the tail in a TS6–7 embryo of Haddadus binotatus (A), and TS5 embryos of Oreobates sp. (B) and O. barituensis (C). The small line drawings highlight the arrangement of components of the tail: the notochord (white ellipse), neural tube (gray), and muscle anlagen (black).
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