Javier Goldberg

Heterochrony During Skeletal Development of Pseudis platensis (Anura, Hylidae) and the Early Offset of Skeleton Development and Growth

The aquatic frog Pseudis platensis has a giant tadpole, long developmental time, and dissociated metamorphic events that include later offset of larval somatic morphologies. Moreover, when the tadpole metamorphoses, the young frog is nearly the size of an adult, suggesting that this species has low rates of postmetamorphic growth. Herein, we study the development of the skeleton during larval development up to the end of metamorphosis, which is denoted by the complete lost of the tail in P. platensis. Our study revealed heterochronic differences in skeletal development compared with that of most anurans; these involve the complete differentiation of skull bones and the extensive ossification of the postcranial skeleton before completion of metamorphosis. The skull of metamorphosing P. platensis has an ossified sphenethmoid and a fully formed plectral apparatus, thus differing with regard to the pattern observed in most anurans in which both developmental events take place during the postmetamorphic life. Despite the fact that the iliosacral articulation and the urostyle are present at the end of metamorphosis as in most anurans, ossification/calcification of carpus, tarsus, and limb epihyses during metamorphosis of P. platensis suggests that the postcranial skeleton lacks postmetamorphic growth. This study also includes a discussion of the pattern of development of the plectral apparatus, which allows us to propose a new hypothesis regarding pars externa plectri homology. J. Morphol., 2009.

Sesamoids in Anurans: New Data, Old Issues

Sesamoids are skeletal elements rarely considered in studies of the vertebrate skeleton. In this work, we integrate ontogenetic data of anuran sesamoids in two species (Leptodactylus latinasus and Pleurodema cf. guayapae), the related structures (tendons, muscles, and joints) in L. latinasus, and a survey of sesamoid distribution in 185 anuran taxa. Our main goals are: (1) to contribute to the knowledge of the comparative anatomy of sesamoids in tetrapods; (2) to provide additional developmental evidence to interpret the ontogenetic pattern of sesamoids in anurans, as a key to elucidate that of tetrapods in general; (3) to provide data about tendon development in relation to sesamoid development in anurans for the first time; and (4) to propose a pattern of anuran sesamoid distribution. The homologies of sesamoids across tetrapods are discussed here. Observations were made in cleared and stained skeletal whole‐mounts. Fifty‐four sesamoids were found in anurans, thirty‐seven of which occur in L. latinasus. The traditional point of view of embedded sesamoids always resulting from biomechanical stimuli of a previously existing tendon is not sustained by our data. Many sesamoids arise before the differentiation of a tendinous tissue. Our survey results in a data set where the two big anuran clades, Hyloides (12 families) and Ranoides (14 families), were represented. The matrix has 38% missing entries. Most of the surveyed sesamoids have multiple origins, with only three of them (about 19%) having one origin. Anat Rec 293:1646–1668, 2010.

Giant Tadpole and Delayed Metamorphosis of Pseudis platensis Gallardo, 1961 (Anura, Hylidae)

Abstract Pseudis platensis, like Pseudis paradoxa, is a Neotropical aquatic frog with a giant tadpole. Despite being one of the few anuran species whose larvae grow larger than adults, knowledge of its larval development is limited to prometamorphic stages. This study describes qualitative and quantitative variation through P. platensis larval development, including descriptions of various traits (lateral line, oral disc, vent tube, limbs) and their transformations during metamorphosis. We found similarities with the development of other anurans at larval stages up to the end of prometamorphosis but not with their metamorphic stages. For this species, we described key features to characterize 13 ontogenetic stages as follows: four for prometamorphic larval morphologies, eight stages covering metamorphic changes, and one defining the posmetamorphic adult stage. At the end of prometamorphosis, tadpole body size in P. platensis is similar to adult size, but the tail shows extra development. Unlike most anurans, the disappearance of two larval traits (i.e., vent tube and tail) is delayed until later in metamorphosis. Larval development of P. platensis exhibits unique features not reported for other anurans and offers a model to study developmental and evolutionary aspects of anuran metamorphosis.

The Development of Dermatonotus muelleri (Anura: Microhylidae: Gastrophryninae)

Abstract The monophyly of Microhylidae is supported by an overwhelming accumulation of synapomorphic larval features. Despite the distinctiveness of the microhylid tadpole, few studies have focused on larval development. Microhylid larval morphology is usually described and based on standard tables that imply that developmental events at equivalent stages of overall tadpole development are independent from species-specific patterns of developmental timing. Herein, we present additional developmental data based on external morphology and field data on larval growth for the gastrophrynine microhylidDermatonotus muelleri. We describe internal morphological variation (e.g., skeletal and soft systems) during larval development. The results indicate that the onset of some metamorphic changes occur earlier than those implied in current anuran developmental tables. This study provides baseline information for microhylid species that will allow comparisons of ontogenetic trajectories, heterochronic patterns influencing larval body plan, and the role of larval morphology on the adult microhylid body plan.

The ontogeny of Pseudis platensis (Anura, Hylidae): Heterochrony and the effects of larval development on postmetamorphic life

Recent studies have described the giant tadpole, delayed metamorphic transformations, and absence of postmetamorphic growth of the skeleton of Pseudis Platensis. These features address questions about derived patterns of life cycles and the role of the heterochrony during the metamorphosis in anurans. Using anatomical methods, we provide new data on the development of reproductive, digestive and integument systems, and age inference obtained from ontogenetic series of Pseudis platensis. Our results indicate that at the end of metamorphosis, the adult skin is completely differentiated, including the calcified dermal layer; the testis has seminiferous tubules with spermatogonia, spermatocytes, and spermatids; ovarian sacs present previtellogenic ova; and the adult digestive tract is fully formed. The froglets differ from adults only in being unable to reproduce. The entire life cycle of P. platensis can occur in 4 years. In the first year, larval development, growth to adult size, and gonad differentiation are completed. Long larval development rather than size of the tadpoles seems to be involved in the absence of juvenile stages. J. Morphol., 2010.

Developmental changes and novelties in ceratophryid frogs

Abstract The Neotropical frog genera Ceratophrys, Chacophrys and Lepidobatrachus form the monophyletic family Ceratophryidae. Although in- and out-group relationships are not fully resolved, the monophyly of the three genera is well supported by both morphological and molecular data. Much is known about the morphology of the ceratophryids, but there is little comparative information on how modification of a common ancestral developmental pathway played a role in shaping their particular body plans. Herein, we review morphological variation during ceratophryid ontogeny in order to explore the role of development in their evolution. The ceratophryids are collectively characterized by rapid larval development with respect to other anurans, yet the three genera differ in their postmetamorphic growth rates to sexual maturity. Derived traits in the group can be divided into many homoplastic features that evolved in parallel with those of anurans with fossorial/burrowing behaviors in semiarid environments, and apomorphies. Morphological novelties have evolved in their feeding mechanism, which makes them capable of feeding on exceptional large prey. Lepidobatrachus is unusual in having reduced the ecomorphological differences between its larvae and adults. As a result, both the larvae and the frog are similarly able to capture large prey underwater. Some unique features in Lepidobatrachus are differentiated in the tadpole and then exaggerated in the adult (e.g., the posterior displaced jaw articulation) in a manner unobserved in any other anurans.

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

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.

A Tale of a Tail: Variation during the Early Ontogeny of Haddadus binotatus (Brachycephaloidea: Craugastoridae) as Compared with Other Direct Developers

Abstract 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. Resumen 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.

Vocal sac development and accelerated sexual maturity in the lesser swimming frog, Pseudis minuta (Anura, Hylidae).

Sexual maturity involves the differentiation of the reproductive system, the maturation of germ cells, and the development of secondary sexual characteristics. Even though this topic has received much attention, little is known about the sequence of events that encompass reproductive maturation in anurans and what it could reveal about the developmental basis of life cycle evolution. The discovery of froglets of Pseudis minuta with incipient vocal sacs calling in breeding pools alongside several larger adult specimens with fully developed vocal sacs raised the question of the timing of sexual maturity in this species. Here we describe the sequence and timing of differentiation, development and maturation of the vocal sac apparatus and the testes in P. minuta (Anura, Hylidae), in order to establish a timeline of events leading to sexual maturity. Differentiation of the vocal sac apparatus begins at the final metamorphic stages, earlier than reported for other species, and the vocal sac acquires its final shape during the early postmetamorphic period. These modifications occur after gonadal differentiation, which begins early during the larval period and proceeds with a highly accelerated rate of development (e.g., secondary spermatids appear well before metamorphic climax), a situation reported previously for other anuran species only in the genus Pseudis. These results, together with a skeletochronological analysis showing that some calling specimens presented no lines of arrested growth, indicate acceleration in the timing of sexual maturity in Pseudis, and raise questions about the interdependence/decoupling during the development of the different components involved in reaching the adult stage.

Gonadal Differentiation and Development in the Snouted Treefrog, Scinax fuscovarius (Amphibia, Anura, Hylidae)

Abstract Accurate descriptions of gonadogenesis are necessary to have a baseline to detect abnormalities during development and to assess the time a species may be more vulnerable to the action of pesticides, endocrine disruptors, and pharmaceuticals to which abnormal conditions have been attributed. Here, I describe the histomorphological changes during gonadal differentiation in the Snouted Treefrog Scinax fuscovarius. I sexed and measured a total of 302 tadpoles between Gosner stages 26–46 and 21 juvenile and adults. The results show that 1) the species possesses the undifferentiated type of gonadal differentiation—ovaries differentiate much earlier (at stage 26) than testes (stage 36); 2) oogenesis begins almost simultaneously with ovarian differentiation; and 3) ovaries and testes exhibit different rates of gonadal differentiation with respect to somatic development—the ovaries have an accelerated rate (the ovarian cavity differentiates early during larval development and previtellogenic oocytes develop at early premetamorphic stages), whereas the testes have a decelerated rate (seminiferous tubules differentiate at the juvenile stage). The comparison of these characteristics with those of other co-occurring anuran species reveals important interspecific variation in the relative timing of gonadogenesis. Finally, and as a byproduct of the extensive sampling, I describe several cases of gonadal malformations.