Marissa Fabrezi

Developmental Basis of Limb Homology in Lizards

Shubin and Alberch (Evol Biol 1986 ;20:319–387) proposed a scheme of tetrapod limb development based on cartilage morphogenesis that provides the arguments to interpret the homologies of skeletal elements and sets the basis to explain limb specialization through later developmental modification. Morphogenetic evidence emerged from the study of some reptiles, but the availability of data for lizards is limited. Here, the study of adult skeletal variation in 41 lizard taxa and ontogeny in species of Liolaemus and Tupinambis attempts to fill in this gap and provides supporting evidence for the Shubin‐Alberch scheme. Six questions are explored. Is there an intermedium in the carpus? Are there two centralia in the carpus? Is there homology among proximal tarsalia of reptiles? Does digit V belong to the digital arch? Is the pisiform an element of the autopodium plan? And should the ossification processes be similar to cartilage morphogenesis? We found the following answers. Some taxa exhibit an ossified element that could represent an intermedium. There is one centrale in the carpus. Development of proximal tarsalia seems to be equivalent with that observed among reptiles. Digit V could arise from the digital arch. Pisiform does not arise as part of the limb plan. And different patterns of ossification occur following a single and conservative cartilaginous configuration. Lizard limb development shows an early pattern common to other reptiles with clear primary axis and digital arch. The pattern then becomes lizard‐specific with specialization involving some reduction in prechondrogenic elements. Anat Rec 2007.

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.

Parallelism and convergence in anuran fangs

The anuran lower jaw is composed of three pairs of bones: dentaries, angulosplenials and mentomeckelians. Although the lower jaw is toothless, except in Gastrotheca guentheri, enlarged fangs or odontoids have evolved at least four times independently in some myobatrachids, hylids, ranids and leptodactylids through both parallel and convergent evolutionary events. Fangs seem to represent the single best design solution to enable an anuran to inflict a bite-like wound, but the biological role of biting varies among species. Fangs are projections of the dentaries in ranids, but in the hylid frog Hemiphractus and in ceratophryine leptodactylids, they form a sinosteotic unit with the dentaries and mentomeckelians. Comparisons of morphology, behaviour and diet among frog taxa with enlarged fangs reveal that the fangs may be the result of either sexual or natural selection. Those fangs that evolved in response to sexual selection seem to be relatively larger than those that resulted of natural selection.

Heterochrony in Growth and Development in Anurans from the Chaco of South America

Heterochrony refers to those permutations in timing of differentiation events, and those changes in rates of growth and development through which morphological changes and novelties originate during phyletic evolution. This research analyzes morphological variation during the ontogeny of 18 different anuran species that inhabit semi-arid environments of the Chaco in South America. I use field data, collection samples, and anatomical methods to compare larval growth, and sequences of ontogenetic events. Most species present a similar pattern of larval development, with a size at metamorphosis related to the duration of larval period, and disappearance and transformations of larval features that occur in a short period between forelimb emergence and tail loss. Among these 18 species, Pseudisparadoxa has giant tadpole and long larval development that are the results of deviations of rates of growth. In this species events of differentiation that usually occur at postmetamorphic stages have an offset when tail is still present. Tadpoles of Lepidobatrachus spp. reach large sizes at metamorphosis by accelerate developmental rates and exhibit an early onset of metamorphic features. The uniqueness of the ontogeny of Lepidobatrachus indicates that evolution of anuran larval development may occasionally involve mid-metamorphic morphologies conserving a free feeding tadpole and reduction of the morphological-ecological differences between tadpoles and adults.

Intercalary Elements, Treefrogs, and the Early Differentiation of a Complex System in the Neobatrachia

Intercalary elements are additional skeletal structures of digits of many anuran amphibians. Twelve terminal clades in the neobatrachian lineage of frogs have intercalary elements revealing it is a homoplastic character with five to seven gains and two to four losses along a consensus phylogeny of the Neobatrachia. We analyzed anatomical variation of intercalary elements, related structures (distal phalanges, tendons, and muscles), and articulations of digits of 45 anuran species, representing eight suprageneric terminal taxa. The intercalary elements are integrated in a complex system that is probably related to different types of movements, which are produced by a similar set of muscles and tendons with limited variation among the studied taxa. Species in the clades Hyloides and Ranoides show distinctive patterns of morphostructural features in their intercalary elements that are usually wedge‐shaped and composed of hyaline cartilage in Ranoides, and biconcave and composed of embryonic cartilage in Hyloides. Features derived from the typical hyloid condition may only be interpreted in some Hylidae (Pseudis and Lysapsus) and Centrolenidae. In Ranoides, the described features of the intercalary elements are found in all taxa examined with the exception of Leptopelis, which have an intercalary element similar to the other Ranoides but formed by connective tissue. Several features are shared by all taxa having intercalary elements: (1) the intercalary elements differ from the phalanges by lacking terminal epiphyses, (2) they are present in hands and feet, and (3) they appear in all digits. This finding suggests that the genetic basis for presence of intercalary elements may be homologous in all these taxa and may have evolved only once early in neobatrachian history. Anat Rec, 2007.

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.

Hyoid Skeleton, Its Related Muscles, and Morphological Novelties in the Frog Lepidobatrachus (Anura, Ceratophryidae)

Many traits of the skull of ceratophryines are related to the capture of large prey independently of aquatic or terrestrial feeding. Herein, detailed descriptions of the development of hyoid skeleton and the anatomy of muscles responsible for hyoid and tongue movements in Lepidobatrachus laevis and L. llanensis are provided and compared with those of other neobatrachians. The aquatic Lepidobatrachus has special features in its hyoid skeleton that integrates a set of derived features convergent with the conditions observed in non‐neobatrachian anurans and morphological novelties (e.g., dorsal dermal hyoid ossification) that deviate from the generalized pattern found in most frogs. Further, reduction of fibers of muscles of buccal floor, reduction or loss of hyoid muscles (m. geniohyoideus rama lateralis, anterior pair of m. petrohyoideus posteriores), small tongue, and simplified tongue muscles are also morphological deviations from the pattern of terrestrial ceratophryines, and other aquatic ceratophryids (e.g., Telmatobius) that seem to be related to feeding underwater. The historical derived features shared with Chacophrys and Ceratophrys involved in megalophagy are conserved in Lepidobatrachus and morphological changes in the hyoglossal apparatus define a unique functional complex among anurans. Anat Rec, 292:1700–1712, 2009.

Anuran Locomotion: Ontogeny and Morphological Variation of a Distinctive Set of Muscles

Adult morphological variation of muscles originating on the iliac shaft (M. iliacus externus, M. internus, and tensor fasciae latae) and vertebrae (M. longissimus dorsi, M. coccygeosacralis, and M. coccygeoiliacus) that are involved in postmetamorphic anuran locomotion was recorded in 41 neobatrachians and coded in 13 more based on the literature, for a total of 54 anuran species. In addition, we explored the spatial and temporal sequences in the ontogeny of these set of muscles from larval series of 19 neobatrachians whose adults differ in locomotion and lifestyle. Our findings suggest that: (1) jumping, swimming, and/or walking are capabilities that could have been achieved from novelties of limbs and protractor muscles of the femur rather than from changes in the axial musculoskeletal system; (2) the initial ontogenetic phase of the locomotion comprises the capability to escape, when the tail is still present; (3) the secondary phase of locomotion comprises changes in the axial skeleton and muscles integrated to the pelvis and might develop simultaneously with the new feeding mechanism of the recently metamorphosed frog.

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.

Ontogenetic and Structural Variation of Mineralizations and Ossifications in the Integument within Ceratophryid Frogs (Anura, Ceratophryidae)

Ceratophryidae represent a monophyletic group of terrestrial and aquatic frogs inhabiting lowlands of South America where they are more diverse in semiarid environments of the Chaco region. Adult morphology of ceratophryids presents some features associated to terrestrial and fossorial life such as hyper‐ossified skulls, spade feet for digging, among others. For anurans, different mineralized structures have been described in the integument as calcium reservoirs and related to the terrestrial life and water balance (e.g., the calcified layer and dermal ossifications). We describe the ontogeny of the integument in the three genera of ceratophryids (Chacophrys, Ceratophrys, and Lepidobatrachus) that inhabit in semiarid environments. Data obtained demonstrated the early acquisition of metamorphic transformations in the integument layers in larvae of Ceratophrys cranwelli and Lepidobatrachus spp. and a continuous increment in the thickness of them up to old postmetamorphic stages. The integument of ceratophryids develops calcium deposits as the calcified layer during postmetamorphic stages. Furthermore, dorsal shields are also present in adult stages independently of terrestrial versus aquatic lifestyles. While the calcified layer seems to be a feature of a fully developed integument, in which their layers have acquired the adult thickness, dorsal shields develop at premetamorphic stages in L. llanensis and postmetamorphic individuals of C. cranwelli. In ceratophryids, similar to other studied taxa (e.g., Brachycephalus spp.) dorsal shields develop via an intramembranous ossification in which the calcified layer does not precede its differentiation. Within anurans, the occurrence of dorsal shields in the monophyletic ceratophryids suggested a distinctive evolutionary history in the lineage. Anat Rec, 2012.