Frogs at the summits: phylogeny of the Andean frogs of the genus Telmatobius (Anura, Telmatobiidae) based on phenotypic characters.

A phylogenetic hypothesis for the frogs of the genus Telmatobius that includes a comprehensive sample of the morphological and geographical variation is lacking. Obtaining such a hypothesis constitutes the main focus of this contribution. A phylogenetic matrix was generated based on 97 phenotypic characters and 56 terminals. A parsimony analysis of this matrix was performed with TNT. Telmatobius is found to be monophyletic and well supported by 11 synapomorphies. Although the consensus tree shows several polytomies, four main groups have been recovered. The well-supported T. verrucosus Group includes forest and sub-paramo species from Bolivia and Peru, and is the sister group of the remaining species. The T. bolivianus Group includes forest and inter-Andean valley species from Argentina and Bolivia but it is poorly supported. Two supported high-altitude groups have been recovered, the T. macrostomus Group from the Central Andes of Peru, and the T. marmoratus Group from the Altiplano-Puna Plateau of Argentina, Bolivia, Peru and Chile and its adjacent Pacific and Northern slopes. The synapomorphies proposed for Telmatobius are discussed as well as the evolution of some of these synapomorphies and other characters within the genus.

Back to the water: Tongue morphology associated to contrasting lifestyles in two Andean frogs of the genus Telmatobius.

The evolution of the tongue in tetrapods is associated with feeding in the terrestrial environment. This study analyzes the tongue morphology of two closely related frog species, Telmatobius oxycephalus and T. rubigo, which exhibit contrasting feeding mechanisms. Telmatobius oxycephalus, a semi-aquatic species, relies on its tongue to capture terrestrial prey whereas T. rubigo, a secondarily aquatic species, uses suction feeding not involving the tongue. Through anatomical, histological and scanning electron microscopy analyses, we revealed remarkable differences in tongue morphology between these species. Telmatobius oxycephalus exhibits a well-developed tongue whose dorsal epithelium has numerous and slender filiform papillae. The epithelial cells of the papillae are protruded and have a complex array of microridges. In contrast, T. rubigo possesses a reduced tongue with flat and less numerous filiform papillae. The epithelial cells are completely flat and lack microridges. These findings highlight the remarkable adaptability of lingual morphology in Telmatobius to respond to the contrasting ecological niches and prey capture mechanisms. This study sheds light on the relationship between tongue shape and the different functional demands, contributing to our understanding of the evolution of prey capture mechanisms in amphibians.

Vascularization inside the epidermis of Neotropical anurans (Nobleobatrachia).

Anuran skin is a dynamic organ involved in essential functions that strongly correlate with specific morphological traits. Particularly, gas exchange has been associated with epidermal modifications, such as reduced cell layers and increased vascularization. Here, we describe the epidermal morphology and its association with capillary networks in the dorsal skin of 103 Neotropical anurans (Nobleobatrachia) from different ecomorphs and habitats. Additionally, we examined the lateral and ventral skin for a subset of these species. We report intraepidermal capillaries in (i) dorsal skin of Lepidobatrachus laevis and Lepidobatrachus llanensis (burrowing and semi-aquatic Chacoan species), Hyloscirtus colymba and Hyloscirtus palmeri (arboreal species from humid forests), and Alsodes neuquensis and 15 Telmatobius spp. (aquatic and semi-aquatic species from cold environments); (ii) lateral skin of Boana benitezi and H. colymba (arboreal species from humid forests), and (iii) ventral skin of B. benitezi, H. colymba, Atelognathus patagonicus (aquatic species from cold environments), and four Chacoan species, Chacophrys pierottii, Ceratophrys cranwelli (burrowing/terrestrial species), and Lepidobatrachus asper and L. llanensis (burrowing/semi-aquatic species). Also, verrucae hydrophilicae were observed exclusively in the ventral skin of Leptodactylus fuscus, Leptodactylus laticeps (terrestrial and Chacoan species), and B. benitezi. Regardless of the skin region, the capillaries always penetrate the epidermis from the dermis, while epidermal cell layers are flattened. Our findings support previous hypotheses stating that the environment where species occur influences skin changes related to cutaneous respiration (intraepidermal capillaries in different body regions) and water absorption (intraepidermal capillaries associated with verrucae hydrophilicae within ventral skin). Also, phylogeny might influence the development of these structures, as revealed by the presence of intraepidermal capillaries in almost all analyzed species of Telmatobius. Finally, the co-occurrence of verrucae hydrophilicae in the ventral skin of hylids from humid forests, and leptodactylids from the subhumid Chacoan region suggest an independent origin.

Phalanx morphology in salamanders: A reflection of microhabitat use, life cycle or evolutionary constraints?

Morphological patterns are modeled by the interaction of functional, phylogenetic, ecological, and/or developmental constraints. In addition, the evolution of life cycle complexity can favor phenotypic diversity; however, the correlation between stages of development may constrain the evolution of some organs. Salamanders present microhabitat and life cycle diversity, providing an excellent framework for testing how these factors constrain phenotypic evolution. We reconstructed the morphological evolution of the terminal phalanx using a sample of 60 extinct and living species of salamanders. Using a geometric morphometric approach combined with comparative analyses, we further investigated the impact of phylogenetic, ecological, and/or life cycle factors on the shape of the terminal phalanx. We find that the phylogeny has some influence in determining the dorsal shape of the phalanges; whereas a relationship between microhabitat or life cycle and the dorsal and lateral shapes of the phalanx was not observed in the analyzed species. The allometric pattern found in the phalanx shape implies that small phalanges are more curved and with more truncated end than bigger phalanges. The evolutionary rate of phalanx shape was higher in the semiaquatic species, and the morphological disparity was significantly higher on biphasic groups. These results contradict the hypothesis that a complex life cycle constrains body shape. Finally, the phalanx shape of the salamander remains quite conserved from the Mesozoic. This configuration would allow them to occur in the different microhabitats occupied by the salamander lineages.

Variation in the growth and development of the hind limbs in frogs of the genus Telmatobius (Anura: Telmatobiidae).

There are remarkable interspecific differences in the sizes of the larvae of Andean frogs of the genus Telmatobius. This size variation seems to be associated with the duration of the larval stage and may affect the hind-limb morphology in Telmatobius. Larval, juvenile, and adult Telmatobius rubigo and T. oxycephalus were examined to determine the variation in relative sizes of hind-limb elements, their growth patterns during postmetamorphic life, and skeletal ontogeny. The results showed that the proportionately shorter hind limbs of T. rubigo relative to those of T. oxycephalus are associated with the protracted development and ossification of hind limbs during the prolonged larval life of T. rubigo. Postmetamorphically, the hind limbs grew faster than the body in juveniles of both species in contrast to the relative growth rates of the hind limbs and bodies of the adults. The growth phase of juvenile T. rubigo seems shorter than that of juvenile T. oxycephalus; possibly, this heightens the difference in the relative lengths of hind limbs after metamorphosis. Temperature affects the effects of thyroid hormone on growth and development, and T. rubigo lives at much higher, colder elevations than does T. oxycephalus. It is not clear whether the developmental differences described here are plastic (i.e., environmentally induced) or genetically fixed in each species.

First record of chytridiomycosis in Bolivia (Rhinella quechua; Anura: Bufonidae).

The finding of tadpoles of Rhinella quechua (Huayramayu River, Carrasco National Park, Cochabamba, Bolivia) with oral abnormalities caused by Batrachochytrium dendrobatidis constitutes the first record of this fungal infection reported for Bolivian amphibians.

Growth and cranial development in the Andean frogs of the genus Telmatobius (Anura: Telmatobiidae): Exploring the relation of heterochrony and skeletal diversity.

Andean frogs of the genus Telmatobius occur at high elevations, they have an aquatic mode of life and large tadpoles. There are more than 60 species that closely resemble one another and have low values of genetic divergence. However, the skeleton, particularly the cranium, is interspecifically variable with respect to the different levels of development of some elements. Heterochrony is considered to have played a prominent role in generating phenotypic variation, especially among closely related species. Herein, the developmental origins of the adult cranial configuration of two species of Telmatobius are explored. The interactions among larval and postmetamorphic growth, sexual maturation, and ossification sequence in T. oxycephalus and T. rubigo are studied. Although there are no substantial changes in the sequences of ossification of the cranium, it is likely that differential timing of larval periods is related to adult cranial characters. The prolonged larval development of T. rubigo may result in peramorphic configurations of bones that ossify during pre-metamorphosis. This long developmental time would also explain why the gonads of T. rubigo are highly differentiated by the end of metamorphosis. In this species, sexual maturation may be attained precociously in relation to metamorphosis, thereby reducing postmetamorphic developmental time of late-onset bones, which have paedomorphic configurations (e.g., vomer, neopalatine, and columella). An inverse pattern characterizes T. oxycephalus, suggesting that the duration of larval life is related to skeletal configuration in Telmatobius.

Morphometric Variations in the Skin Layers of Frogs: An Exploration Into Their Relation With Ecological Parameters in Leptodactylus (Anura, Leptodactylidae), With an Emphasis on the Eberth-Kastschenko Layer.

Leptodactylus is a genus of frogs known to live in diverse habitats and to show both aquatic and terrestrial breeding habits. We studied 21 species of Leptodactylus to explore whether skin structure specialization relates to habitats and habit variation. Morphometric analyses of the skin thickness revealed that phylogeny has a strong influence on variations in the thickness of the epidermis, stratum spongiosum, Eberth-Kastschenko layer, and stratum compactum, while habitat and habits display no significant correlation. The optimization of the phylogenetic hypothesis suggested that a pattern of intermediate values for skin layer thickness are plesiomorphic for this group. Anat Rec, 2017. © 2017 Wiley Periodicals, Inc. Anat Rec, 300:1895-1909, 2017. © 2017 Wiley Periodicals, Inc.

The complex evolutionary history of the tympanic middle ear in frogs and toads (Anura).

Most anurans possess a tympanic middle ear (TME) that transmits sound waves to the inner ear; however, numerous species lack some or all TME components. To understand the evolution of these structures, we undertook a comprehensive assessment of their occurrence across anurans and performed ancestral character state reconstructions. Our analysis indicates that the TME was completely lost at least 38 independent times in Anura. The inferred evolutionary history of the TME is exceptionally complex in true toads (Bufonidae), where it was lost in the most recent common ancestor, preceding a radiation of >150 earless species. Following that initial loss, independent regains of some or all TME structures were inferred within two minor clades and in a radiation of >400 species. The reappearance of the TME in the latter clade was followed by at least 10 losses of the entire TME. The many losses and gains of the TME in anurans is unparalleled among tetrapods. Our results show that anurans, and especially bufonid toads, are an excellent model to study the behavioural correlates of earlessness, extratympanic sound pathways, and the genetic and developmental mechanisms that underlie the morphogenesis of TME structures.

Osteology and postmetamorphic development of Telmatobius oxycephalus (Anura: Telmatobiidae) with an analysis of skeletal variation in the genus.

The osteological diversity among species of Telmatobius has been considered conservative. Nonetheless, the degree of ossification of several features varies both intraspecifically and interspecifically. Herein, intraspecific osteological variation and postmetamorphic ontogenetic changes in osteological features are described in Telmatobius oxycephalus. These data are compared with published descriptions of congeners. There is a considerable intraspecific osteological variation in T. oxycephalus, with cranial characters varying polymorphically, and the hyoid and postcranial characters being sexually dimorphic. This intraspecific variation is expressed by subtle differences in the degree of ossification or mineralization. Interspecific variation also can be described in terms of differential development of osteological features; these differences are more obvious than intraspecifically variable characters. The adult skeletons of several species of Telmatobius resemble the morphology observed in early stages of postmetamorphic development of T. oxycephalus. This is especially evident in the neopalatines, parasphenoid, sphenethmoid, exoccipitals, prootics, vomers, nasals, and plectra. These results suggest that within the conservative osteological architecture of Telmatobius, the variation observed is the result of heterochronic changes during the ossification process.