Exploring the Influence of Neomorphic Gekkotan Paraphalanges on Limb Modularity and Integration.

Digital specializations of geckos are widely associated with their climbing abilities. A recurring feature that has independently emerged within the sister families Gekkonidae and Phyllodactylidae is the presence of neomorphic paraphalanges (PPEs), usually paired, paraxial skeletal structures lying adjacent to interphalangeal and metapodial-phalangeal joints. The incorporation of PPEs into gekkotan autopodia has the potential to modify the modularity and integration of the ancestral limb pattern by affecting information flow among skeletal limb parts. Here we explore the influence of PPEs on limb organization using anatomical networks. We modeled the fore- and hindlimbs in species ancestrally devoid of PPEs (Iguana iguana and Gekko gecko) and paraphalanx-bearing species (Hemidactylus mabouia and Uroplatus fimbriatus). To further clarify the impact of PPEs we also expunged PPEs from paraphalanx-bearing network models. We found that PPEs significantly increase modularity, giving rise to tightly integrated sub-modules along the digits, suggesting functional specialization. Species-specific singularities also emerged, such as the trade-off between the presence of PPEs favoring modularity (along the proximodistal axis) and the interdigital webbing favoring integration (across the lateromedial axis) in the limbs of U. fimbriatus. The PPEs are characterized by low connectivity compared with other skeletal elements; nevertheless, this varies based on their specific location and seemingly reflects developmental constraints. Our results also highlight the importance of the fifth metatarsal in generating a shift in lepidosaurian hindlimb polarity that contrasts with the more symmetrical bauplan of tetrapods. Our findings support extensive modification of the autopodial system in association with the addition of the neomorphic and intriguing PPEs.

Phylogenetic patterns and correlation of key structures for jumping: bone crests and cross-sectional areas of muscles in Leptodactylus (Anura, Leptodactylidae).

Anurans are characterized by their saltatory mode of locomotion, which is associated with a specific morphology. The coordinated action of the muscles and bones of the pelvic girdle is key to the transmission of the force of the hindlimbs to the axial skeleton during jumping. Two features are critical for optimal locomotory performance: the cross-sectional area of muscle and the bone crest attachment sites. The first character is a proxy of the force exerted by the muscle, whereas the crests are muscle attachments sites related to muscle force. The provisory relationship between these features has previously been identified and bone crest size can be used to infer the magnitude and, therefore, muscle force in fossils records. In this work, we explore the correlation between the cross-sectional area of essential muscles to the jumping mechanism (longissimus dorsi, extensor iliotibialis B, tenuissimus, puboischiofemoralis internus B, coccygeo-sacralis and coccygeo-iliacus) and the bone crests where these muscles are inserted (dorsal tubercle, dorsal crest and urostylar crest) in species of the genus Leptodactylus. This genus, along with other leptodactylids, exhibits a diversity of locomotor modes, including jumping, hopping, swimming and burrowing. We therefore analyzed the morphometric variation in the two features, cross-sectional area and bone crest area, expecting a correlation with different locomotor types. Our results showed: (i) a correlation between the urostylar crest and the cross-sectional area of the related muscles; (ii) that the bone crest surface area of urostyle and ilium and the cross-sectional area of the corresponding muscles can be utilized to infer locomotor faculties in leptodactylid frogs; and (iii) that the evolution of both characters demonstrates a general tendency from lower values in leptodactylid ancestors to higher values in the Leptodactylus genus. The results attest to the importance of the comparison of current ecological and phylogenetic analogues as they allow us to infer functionality and behavior in fossil and extant groups based on skeletal evidence. Phylogenetic patterns in character evolution and their correlation with locomotory types could imply that functional restrictions are also inherited in leptodactylid.

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.

Delimiting the boundaries of sesamoid identities under the network theory framework.

Sesamoid identity has long been the focus of debate, and how they are linked to other elements of the skeleton has often been considered relevant to their definition. A driving hypothesis of our work was that sesamoids' nature relies deeply on their connections, and thus we propose an explicit network framework to investigate this subject in Leptodactylus latinasus (Anura: Leptodactylidae). Through the dissection of L. latinasus' skeleton, we modeled its anatomical network where skeletal elements were considered nodes while joints, muscles, tendons, and aponeurosis were considered links. The skeletal elements were categorized into canonical skeletal pieces, embedded sesamoids, and glide sesamoids. We inquired about the general network characterization and we have explored further into sesamoid connectivity behavior. We found that the network is structured in a modular hierarchical organization, with five modules on the first level and two modules on the second one. The modules reflect a functional, rather than a topological proximity clustering of the skeleton. The 25 sesamoid pieces are members of four of the first-level modules. Node parameters (centrality indicators) showed that: (i) sesamoids are, in general terms, peripheral elements of the skeleton, loosely connected to the canonical bone structures; (ii) embedded sesamoids are not significantly distinguishable from canonical skeletal elements; and (iii) glide sesamoids exhibit the lowest centrality values and strongly differ from both canonical skeletal elements and embedded sesamoids. The loose connectivity pattern of sesamoids, especially glides, could be related to their evolvability, which in turn seems to be reflected in their morphological variation and facultative expression. Based on the connectivity differences among skeletal categories found in our study, an open question remains: can embedded and glide sesamoids be defined under the same criteria? This study presents a new approach to the study of sesamoid identity and to the knowledge of their morphological evolution.

Sesamoids in tetrapods: the origin of new skeletal morphologies.

Along with supernumerary bones, sesamoids, defined as any organized intratendinous/intraligamentous structure, including those composed of fibrocartilage, adjacent to an articulation or joint, have been frequently considered as enigmatic structures associated with the joints of the skeletal system of vertebrates. This review allows us to propose a dynamic model to account for part of skeletal phenotypic diversity: during evolution, sesamoids can become displaced, attaching to and detaching from the long bone epiphyses and diaphysis. Epiphyses, apophyses and detached sesamoids are able to transform into each other, contributing to the phenotypic variability of the tetrapod skeleton. This dynamic model is a new paradigm to delineate the contribution of sesamoids to skeletal diversity. Herein, we first present a historical approach to the study of sesamoids, discussing the genetic versus epigenetic theories of their genesis and growth. Second, we construct a dynamic model. Third, we present a summary of literature on sesamoids of the main groups of tetrapods, including veterinary and human clinical contributions, which are the best-studied aspects of sesamoids in recent decades. Finally, we discuss the identity of certain structures that have been labelled as sesamoids despite insufficient formal testing of homology. We also propose a new definition to help the identification of sesamoids in general. This review is particularly timely, given the recent increasing interest and research activity into the developmental biology and mechanics of sesamoids. With this updated and integrative discussion, we hope to pave the way to improve the understanding of sesamoid biology and evolution.

Tendinous framework of anurans reveals an all-purpose morphology.

Tendons are directly associated with movement, amplifying power and reducing muscular work. Taking into account habitat and locomotor challenges faced by anurans, we identify the more conspicuous superficial tendons of a neotropical anuran group and investigate their relation to the former factors. We show that tendons can be visualized as an anatomical framework connected through muscles and/or fascia, and describe the most superficial tendinous layer of the postcranium of Leptodactylus latinasus. To analyze the relation between tendon morphology and ecological characters, we test the relative length ratio of 10 tendon-muscle (t-m) elements in 45 leptodactylid species while taking phylogeny into account. We identify the evolutionary model that best explains our variables. Additionally, we optimize t-m ratio values, and the shape of the longissimus dorsi insertion onto a selected phylogeny of the species. Our data show the existence of an all-purpose morphology that seems to have evolved independently of ecology and functional requirements. This is indicated by no significant relation between morphometric data of the analyzed tendons and habitat use or locomotion, a strong phylogenetic component to most of the analyzed variables, and a generalized pattern of intermediate values for ancestral states. Ornstein-Uhlenbeck is the model that best explains most t-m variables, indicating that stabilizing selection or selective optima might be driving shifts in tendon length within Leptodactylidae. Herein, we show the substantial influence that phylogeny has on tendon morphology, demonstrating that a generalized and stable morphological configuration of tendons is adequate to enable versatile locomotor modes and habitat use. This is an attempt to present the tendinous system as a framework to body support in vertebrates, and can be considered a starting point for further ecomorphological research of this anatomical system in anurans.

Osteology of Physalaemus nattereri (Anura: Leptodactylidae) with comments on intraspecific variation.

The cranium, postcranium, and osteological variation of Physalaemus nattereri (Steindachner) are described. The main sources of variation involve the degree of mineralization of the nasal capsule and the lengths of dermal skull bones (e.g., vomer, sphenethmoid, and neopalatine). Osteologically, P. nattereri differs from its congeners by the anterior placement of the jaw articulation (which lies anterior to the intersection between the alae and cultriform process of parasphenoid), and by the separation of the frontoparietals from the anterior margins of exoccipitals. Descriptions of the nasal capsule, the auditory apparatus, and the iliosacral articulation are presented for the first time for this species. One putative morphological synapomorphy is presented for the P. signifer Clade.

Network architecture associated with the highly specialized hindlimb of frogs.

Network analyses have been increasingly used in the context of comparative vertebrate morphology. The structural units of the vertebrate body are treated as discrete elements (nodes) of a network, whose interactions at their physical contacts (links) determine the phenotypic modules. Here, we use the network approach to study the organization of the locomotor system underlying the hindlimb of frogs. Nodes correspond to fibrous knots, skeletal and muscular units. Edges encode the ligamentous and monoaxial tendinous connections in addition to joints. Our main hypotheses are that: (1) the higher centrality scores (measured as betweenness) are recorded for fibrous elements belonging to the connective system, (2) the organization of the musculoskeletal network belongs to a non-trivial modular architecture and (3) the modules in the hindlimb reflect functional and/or developmental constraints. We confirm all our hypotheses except for the first one, since bones overpass the fibrous knots in terms of centrality. Functionally, there is a correlation between the proximal-to-distal succession of modules and the progressive recruitment of elements involved with the motion of joints during jumping. From a developmental perspective, there is a correspondence between the order of the betweenness scores and the ontogenetic chronology of hindlimbs in tetrapods. Modular architecture seems to be a successful organization, providing of the building blocks on which evolution forges the many different functional specializations that organisms exploit.