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Development and Morphology of Rostral Cartilages in Batoid Fishes (Chondrichthyes: Batoidea), with Comments on Homology Within Vertebrates

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Development and Morphology of Rostral Cartilages in Batoid Fishes (Chondrichthyes: Batoidea), with Comments on Homology Within Vertebrates Biological Journal of the Linnean Society (1992), 46: 259-298. With 17 figures Development and morphology of rostral cartilages in batoid fishes (Chondrichthyes: Batoidea), with comments on homology within vertebrates TSUTOMU MIYAKE, JOHN D. McEACHRAN*, PETER J. WALTON? AND BRIAN K. HALL Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 431, Canada, *Department of Wildlge and Fisheries Sciences, Texas A@M University, College Station, Texas 77843, and ?Baylor College of Medicine, 1 Baylor Plaza, Houston, Texas 77030, U.S.A. Received 30 August 1990, acceptedfor publication 28 November 1990 The rostral cartilages of batoid fishes were examined to elucidate their development, morphology and homology. Comparison of a variety of rostral cartilages among elasmobranchs with other groups of vertebrates shows that rostral cartilages originate embryologically from the trabecula and/or lamina orbitonasalis. Because different morphogenetic patterns of the derivatives of the two embryonic cartilages give rise to a wide variety of forms of rostral cartilages even within elasmobranchs, and because morphogenesis involves complex interactions among participating structures in the ethmo-orbital area, we put forward conceptual and empirical discussions to elucidate the homology of the rostral cartilages in batoid fishes. With six assumptions given in this study and based on recent discussions of biological and historical homology, our discussions centre on: ( 1 ) recognition of complex interactions of participating biological entities in development and evolution; (2) elucidation of a set of interacting biological and evolutionary factors to define a given morphological structure; (3) assessment of causal explanations for similarities or differences between homologous structures by determining genetic, epigenetic and evolutionary factors. Examples of conceptual approaches are given to make the approaches testable. Although a paucity of knowledge of rostral cartilage formation is the major obstacle to thorough analysis of the conceptual framework, several tentative conclusions are made on the homology of rostral cartilages that will hopefully attract more research on development and evolution in vertebrate morphology. These are: (1) the rostral cartilage in each group of vertebrates examined can be defined by both developmentally associated and adult structural attributes, yet such data do not allow us to assess homology of a variety of forms of rostral cartilages at higher taxonomic categories; (2) the entire rostral cartilage in elasmobranchs is formed by the contribution of the embryonic trabecula and lamina orbitonasalis. The status of the development and homology of the rostral cartilage in holocephalans remains uncertain; (3) there is no simple picture of evolution of rostral cartilages among three putative monophyletic assemblages of elasmobranchs, galeomorphs, squaloids (possibly plus Squatina, Chlamydoselachus and hexanchoids as the orbitostylic group) and batoid fishes. It is highly likely that rostral cartilages in each subgroup or subgroups of these assemblages may be of phylogenetic significance but that it may not serve as a basis to unite these assemblages into much higher assemblages; (4) the tripodal rostral cartilage is unique in form in the group including some carcharhinoid and lamnoid sharks. The status of the analogous tripodal cartilage in some squaloids remains uncertain. The unfused tripodal cartilage of the electric ray Narke is interpreted as developmentally equivalent to, but not homologous with, the unfused or fused ones in the sharks; (5) the rostral cartilage in the electric ray Torpedo is uniquely formed because of its embryonic origin solely from the ventro-medial part of the lamina orbitonasalis, but it is regarded as homologous with the rostral cartilages which are formed by the trabecula and other components of the lamina 259 0024-4066/92/070259 + 40 $03.00/0 0 1992 The Linnean Society of London 260 T. MIYAKE ETT AL. orbitonasalis in other batoid fishes; (6) the cornu trabecula contributes to the formation of the ventral stem of the rostral cartilage at least in elasmobranchs, especially to a particular set of rostral cartilages, i.e. the tripodal rostral cartilage in the shark scyliorhinus and dorso-ventrally flattened rostral shaft in the narcinidid electric rays; (7) there is a unique form of a rostral shaft with rostral appendix in skates and probably guitarfishes; (8) there is no rostral cartilage in adult benthic stingrays, pelagic stingrays Dasyatis violacea and Myliobatidae, although it is present in embryonic stages; (9) there is a unique form of the rostral cartilage as a rostral projection from the dorso-lateral part of the lamina orbitonasalis in pelagic stingrays Rhinopteridae and Mobulidae, which together with part of the pectoral fins, forms a pair of cephalic fins; (10) different developmental mechanisms may be responsible for the absence or loss of rostral cartilages in different groups, i.e. absence of the cartilage derived from the medial area of the trabecula in Torpedo vs absence of the rostral cartilage in benthic stingrays; (1 1) the rostral cartilages in some placental mammals (cetaceans and sirenians) arise only from the medial area of the trabecula because monotreme and placental mammals do not form the trabecula cranii; (12) some actinopterygians and sacropterygians possess a rostral cartilage which originates only from the medial area of the trabecula. One scombroid group, including Sardini and Thunnini, Scornberamorus, Acanthocybium, lstiophoridae and Xiphias, possesses a unique larval beak composed of the rostral cartilage, ethmoid cartilage and premaxillar bone. The development and homology of other rostral cartilages remain to be further elucidated; (13) urodeles possess a medial rostral process whose anlage is probably developmentally equivalent to that in batoid fishes but the occurrence in urodeles is either atavistic or unique (autapomorphic); (14) the upper jaw of tadpoles is unique in possessing the suprarostral cartilage; the anlage of the cartilage is probably developmentally equivalent to the outgrowth of the cornu trabecula in batoid fishes. KEY WORDS:--Batoid fishes - craniofacial development - development of rostral cartilage trabecula ~ lamina orbitonasalis - biological and historical homology. CONTENTS Introduction ................... 260 Materials and methods ................ 261 Results .................... 26 1 Cranial embryonic cartilages and formation of rostral cartilages ..... 26 1 Rostral cartilages of skates .............. 263 Rostral cartilages of guitarfishes ............. 265 Rostral cartilages of stingrays .............. 266 Rostral cartilages of sawfishes .............. 269 Rostral cartilages of electric rays ............. 270 Discussion. ................... 274 Development of the trabecula and cornu trabecula. ........ 274 Development of the lamina orbitonasalis ........... 276 Developmental perspectives .............. 279 Homology: assumptions ............... 280 Homology: historical approach ............. 281 Homology: biological approach ............. 286 Homology: conclusions ............... 289 Homology of rostral cartilages .............. 289 Acknowledgements ................. 292 References ................... 293 Abbreviations used in figures ............... 296 Appendix. ................... 297 INTRODUCTION Batoid fishes, one of three major groups of chondrichthyan fishes, comprise more than 450 species and occupy a variety of habitats ranging from freshwater to pelagic and deep benthic marine waters. They consist of five monophyletic groups; electric rays (torpedinoids), sawfishes (pristoids), skates (rajioids), guitarfishes (rhinobatoids) and stingrays (myliobatoids) (Compagno, 1973, 1977). All groups have a dorso-ventrally depressed body with laterally expanded pectoral fins. Their palaeontological history dates back to the Jurassic (Carroll, 1988) and their external morphologies give the impression that they have been morphologically conservative during their long evolution history. However, ROSTRAL CARTILAGES IN BATOID FISHES 26 1 recent systematic and anatomical studies have revealed a variety of anatomical features among the five major groups of batoid fishes (Compagno, 1977; Miyake, 1988; Miyake & McEachran, 1991 ), suggesting major morphological evolution. Recent chromosomal and molecular data support the dynamic nature of their evolutionary history (Ida et al., 1986; Ida, Sat0 & Miyawaki, 1986; Olmo et al., 1982; Schwartz & Maddock, 1986; Stingo, 1979; Stingo & Capriglione, 1986), suggesting considerable karyotypic and molecular changes even within subgroups of batoid fishes (Ida et al., 1986; Schwartz & Maddock, 1986; Stingo & Capriglione, 1986). Miyake (1988) undertook a broad anatomical survey of craniofacial morphologies of batoid fishes and brought attention to many of their evolutionary features. One which has been recognized as of systematic and evolutionary significance is the presence of a rostral cartilage (McEachran & Compango, 1979, 1982; Miyake, 1988). The rostral cartilage is an anterior extension of the cartilaginous neurocranium which is medially sandwiched by the anterior expansion of the pectoral fins (Compagno, 1977; Miyake, 1988). It displays a variety of sizes and shapes, in some cases with an additional cartilaginous appendix at the tip (McEachran & Compagno, 1979, 1982; Miyake, 1988). McEachran & Compagno ( 1982), therefore, placed systematic and phylogenetic emphasis on the morphology
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