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

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Intercalary Elements, Treefrogs, and the Early Differentiation of a Complex System in the Neobatrachia THE ANATOMICAL RECORD 290:1551–1567 (2007) Intercalary Elements, Treefrogs, and the Early Differentiation of a Complex System in the Neobatrachia 1 2 3 ADRIANA S. MANZANO, * MARISSA FABREZI, AND MIGUEL VENCES 1Consejo Nacional de Investigaciones Cientı´ficas y Te´cnicas (CICyTTP-CONICET), Diamante, Entre Rı´os, Repu´ blica Argentina 2Instituto de Bio y Geociencias - Museo de Ciencias Naturales, Universidad Nacional de Salta, Salta, Repu´ blica Argentina 3Zoological Institute, Technical University of Braunschweig, Braunschweig, Germany ABSTRACT 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 var- iation of intercalary elements, related structures (distal phalanges, ten- dons, and muscles), and articulations of digits of 45 anuran species, representing eight suprageneric terminal taxa. The intercalary ele- ments 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 usu- ally 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, 290:1551–1567, 2007. Ó 2007 Wiley-Liss, Inc. Key words: intercalary elements; muscles; digits; treefrogs; anurans Grant sponsor: Agencia Nacional de Promocio´n Cientı´fica y Received 3 April 2007; Accepted 4 September 2007 Tecnolo´gica; Grant number: PICT/2002 12418; Grant sponsor: DOI 10.1002/ar.20608 Consejo Nacional de Investigaciones Cientı´ficas y Te´cnicas; Published online 24 October 2007 in Wiley InterScience (www. Grant number: PIP 6347; Grant sponsor: Universidad Auto´n- interscience.wiley.com). oma de Entre Rı´os; Grant number: PIDP Res. 387-07. *Correspondence to: Adriana S. Manzano, CICyTTP-CONICET, Matteri y Espan˜a, 3105 - Diamante, Entre Rı´os, Repu´blica Argen- tina. Fax: 54-343-4983087. E-mail: [email protected] Ó 2007 WILEY-LISS, INC. 1552 MANZANO ET AL. The intercalary element is an additional skeletal Drewes (1984) noted that hyperoliid and leptopeline structure located between the terminal and subterminal intercalary elements are histologically quite different (penultimate) phalanges in the digits of many anuran from each other. Leptopelinae (Leptopelis) is distin- amphibians. The presence of this element has been guished morphologically by histological distinct interca- hypothesized to be related to other morphological spe- lary phalangeal elements. Rhacophoroidea (Mantellidae cializations associated with arboreal habits, such as well and Rhacophoridae) is a sister group of Ranoidea (Nycti- developed adhesive digit pads (e.g., Paukstis and Brown, batrachidae and Ranidae, sensu stricto), and one charac- 1987, 1991; Wiens et al., 2005). The intercalary may be ter that definitely optimizes on Rhacophoroidea is the part of an integrated system of articulations allowing intercalary element present. angular movements responsible for the attachment and Wiens et al. (2005) found evidence for a significant detachment of the adhesive digit pads (Hanna and influence of homoplasy in the intercalary element on Barnes, 1991). conflicts between morphological and molecular data sets. Analyses of the variation of the intercalary element in These authors characterized the Neotropical family Hyli- frogs were mainly focused on their presence or absence dae by several traits that presumably represent adapta- and resulted in different proposals on the monophyly of tions to the use of arboreal habitat (e.g., expanded toe particular suprageneric groups (Lynch, 1973; Laurent, pads and intercalary elements) and concluded that the 1986; Duellman and Trueb, 1986; Ohler and Dubois, placement of hemiphractines with other hylids may be 1989; Ford and Cannatella, 1993; Duellman, 2001; Frost caused by the convergent acquisition of traits associated et al., 2006). with arboreality (e.g., offset terminal phalanges; claw- Only few studies were carried out on particular line- shaped terminal phalanges, intercalary elements; modi- ages analyzing the variation of the element itself. fied base of metacarpal III), in contrast to the strong Drewes (1984) described four character states in hypero- molecular evidence that hemiphractines are not closely liid frogs on the basis of structural features (juvenile related to other hylids. Several other aspects in a phylo- cartilage without intracellular matrix, cartilaginous and genetic reconstruction based on morphological traits unmineralized, cartilaginous and peripherally mineral- were also seen as possible results of the misleading ized, completely mineralized). Vences et al. (2003) for effects of this suite of traits: (1) the placement of the the same taxon recognized intercalary elements formed clade Centrolenidae 1 Allophryne with hylids, both by cartilage or not and concluded that the degree of min- groups containing taxa with intercalary elements; (2) eralization can differ within a single species and repre- the basal placement of Pseudis, Lysapsus, Acris, and sents only a gradual modification of basically identical some Pseudacris within hylids, which may be associated structures. Scott (2005) in her analysis of ranoid rela- with a reversion to terrestrial and/or aquatic lifestyle in tionships described some variation in the morphology of these clades, with a concomitant loss of one or more of intercalary elements, and Faivovich et al. (2005) consid- the characters associated with arboreality (e.g., offset ered an elongated shape of intercalary elements in Neo- terminal phalanges, expanded toe pads); and (3) the loss tropical treefrogs as a synapomorphy of the clade Lysap- of these traits in the terrestrial/fossorial hylid Cyclorana sus 1 Pseudis, and the partial mineralization of inter- (i.e., terminal phalanges not offset, not claw-shaped, loss calary elements as a synapomorphy of the Scinax of intercalary elements, toe pads not expanded) which catharinae group. may contribute to the erroneous placement of this taxon Paukstis and Brown (1987), studying the intercalary outside of the Hylidae (Wiens et al., 2005). elements in Pseudacris, recognized three morphological Here we present a comparative analysis of different types (wide intercalaries with concave surfaces; cuboi- morphological traits related to intercalary elements in dal intercalaries; and very thin and reduced intercala- representative hyloid and ranoid taxa in which interca- ries), and concluded that reduction of this structure laries are present. Because intercalary elements are could be interpreted as a degenerative condition, fur- morphologically and functionally integrated in anuran ther evolution toward burrowing habits possibly result- limbs, we describe and analyze both (1) the variation in ing in the loss of the intercalary. These authors, shape and structure of the intercalaries and their articu- furthermore, analyzed the correlation between the lations with phalanges, and (2) patterns of variation in morphology of the intercalary elements and the frog’s associated muscles, in particular in the Extensores habits, and hypothesized that the enlargement of the breves profundus, Extensores breves distalis tendons, intercalary could lead to increased digit length for a and Tendo superficialis. Our goal in providing detailed better development of webbing in aquatic species comparative descriptions of these patterns is to obtain a (Paukstis and Brown, 1991). basis for understanding their evolution in the light of Based on the most comprehensive reconstruction of recent phylogenetic hypotheses. amphibian phylogeny (Frost et al., 2006), the occurrence of the intercalary elements is known in five terminal taxa of Hyloides and five terminal taxa of Ranoides, MATERIALS AND METHODS which both are the major lineages in the clade Neobatra- Specimens of 45 species of Neobatrachia with interca- chia (Fig. 1). Frost et al. (2006) reconstructed intercalary lary elements were studied. They belong to eight termi- elements to be synapomorphies for Centrolenidae (Cen- nal suprageneric taxa following the classification troleninae), Microhylidae (Phrynomantis), Artholeptidae proposed by Frost et al. (2006): Amphignathodontidae, (Leptopelinae), and Rhacophoroidea. These authors dis- Hylidae, Centrolenidae, Microhylidae, Mantellidae, cussed intercalary element occurrence and include them Rhacophoridae, Arthroleptidae, and Hyperoliidae.
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