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Downloaded From Developmental morphological diversity in caecilian amphibians: systematic and evolutionary implications Müller, H. Citation Müller, H. (2007, November 8). Developmental morphological diversity in caecilian amphibians: systematic and evolutionary implications. Leiden University Press. Retrieved from https://hdl.handle.net/1887/12462 Version: Corrected Publisher’s Version Licence agreement concerning inclusion of License: doctoral thesis in the Institutional Repository of the University of Leiden Downloaded from: https://hdl.handle.net/1887/12462 Note: To cite this publication please use the final published version (if applicable). Chapter 2 CHAPTER 2 Ontogeny of the skull, lower jaw and hyobranchial skeleton of Hypogeophis rostratus (Amphibia: Gymnophiona: Caeciliidae) revisited Hendrik Müller Department of Zoology, The Natural History Museum, London SW7 5BD, UK and Institute of Biology, Leiden University, Kaiserstraat 63, 2311 GP, Leiden, The Netherlands. KEY WORDS: morphology, direct development, Lissamphibia, ossification sequence, caecilian Published in Journal of Morphology 267: 968–986 (2006) 39 Chapter 2 ABSTRACT Few detailed descriptions of the development of the head skeleton in caecilian amphibians are available. One of those is the work of Marcus and students (e.g., Gehwolf, 1923; Marcus, 1933; Marcus et al., 1935) on the morphology and development of the skull, lower jaw and hyobranchial skeleton in the Seychellean caeciliids Hypogeophis rostratus and Grandisonia alternans. These workers described a high number of individual ossifications that fuse during ontogeny to form the adult skull. Although later studies have doubted the generality of those observations, the work of Marcus and his students has been hugely influential in subsequent studies of caecilian skull morphology and amphibian evolution. Based on new observations on an ontogenetic series of 32 sectioned and cleared and stained specimens, ranging from the beginning of chondrification to the adult, the development of the skull, lower jaw and hyobranchial skeleton of H. rostratus are described. The new results are largely incompatible with those of Marcus and students and no evidence for several of the reported ossifications, including supra-, infra- and basioccipital, epiotic, pleurosphenoid, preethmoid, posterior vomer, prepalatine, quadratojugal, postparietal, second coronoid, supraangular and complementare, is found. It is argued that most of Marcus et al.’s reports of non-existent ossifications are based on false phylogenetic preconception, misinterpretation of the observed morphology and technical error. Data on the ossification sequence of the skull and lower jaw in H. rostratus are provided and briefly compared to published information on Dermophis mexicanus and Gegeneophis ramaswamii. 40 Chapter 2 INTRODUCTION At a time when biosciences as a whole are a fast moving field, morphology and morphological systematics draw both from the most current studies using advanced analytical techniques, as well as from studies that sometimes date back as far as the 19th century. In some cases, such as rare and seldom studied animals for which new material is limited, old accounts often represent the only source of primary morphological data. These, however, as with almost all scientific studies, are the products of their time and are often as much a reflection of contemporary trends as they are documentations of the observed morphology. One possible case in point concerns the skull morphology of caecilian amphibians, where new studies (Wake and Hanken, 1982; Müller et al., 2005) have produced results largely incongruent with earlier studies of skull development (e.g., Marcus et al., 1935). Caecilians (or Gymnophiona), frogs and salamanders constitute the three extant clades of the Amphibia. Caecilians comprise about 170 named species in six families (Wilkinson and Nussbaum, 2005). They are the least known, major living tetrapod clade, which is probably mainly due to their largely subterranean habits and confinement to parts of the wet and seasonal tropics of South and Middle America, Africa and Asia. The first extensive comparative studies of caecilian morphology were undertaken by Wiedersheim (1879) and Peters (1880). Taylor (1969b) provided brief descriptions of adult skull morphology for a broad range of taxa and, most recently, Wake (2003) reviewed and summarized known adult skull morphology of all caecilian genera. However, most studies on caecilian morphology have been restricted to investigations on adult material and were usually carried out on small samples (e.g., Brand, 1956). This led to uncertainties about bone homologies because the heavily ossified, burrowing- adapted caecilian skulls are highly modified compared to the skulls of other amphibians. Little ontogenetic information about caecilians was available when Marcus et al. (1935) published a lengthy account on the development of the skull in what were then thought to be two species of Hypogeophis. Based on their observations 41 Chapter 2 of a very limited number of three ontogenetic stages (early and late embryo and juvenile), they described a high number of individual bones that occur during the development of the skull. These bones were reported to fuse during ontogeny to form a highly compact adult skull that is made up of a relatively small number of bones, like the os basale, which is comprised of the dermal parasphenoid and most of the posterior part of the neurocranium. The formation of the large compound bones from individual ossifications had been already postulated by early students of caecilian skull morphology (Dugès, 1834; Wiedersheim, 1879), and was later corroborated by Peter (1898). However, the unusually high number of separate ossification centers reported by Marcus et al. (1935), aroused much interest (de Beer, 1937) and featured prominently in the still unsettled debate concerning the systematic relationships of living amphibians (Schoch and Milner, 2004 for most recent review). More importantly, because of the general lack of developmental studies in caecilians, the results of Marcus et al. (1935) were seen as representing the standard in caecilian cranial development. Several authors of subsequent studies on caecilian skull morphology (e.g. Ramaswami, 1948; Brand, 1956; Visser, 1963) commented on presumably fused bones, whose presence was assumed rather than actually observed. Some of the results of Marcus et al. (1935) were at least occasionally doubted (Brand, 1956) but were nonetheless largely accepted until Wake and Hanken’s (1982) study of skull development in Dermophis mexicanus, a viviparous Central American caeciliid, in which they were unable to confirm several ossifications (e.g. basi- and supraoccipital, pleurosphenoid, postorbital, quadratojugal) reported by Marcus et al. (1935). Recently, Müller et al. (2005) investigated the development of the skull in the Gegeneophis ramaswamii, an Indian direct-developing caeciliid more closely related to the Seychellean caecilian radiation comprising Hypogeophis rostratus and Grandisonia (Hass et al., 1993; Wilkinson et al., 2002) than Dermophis mexicanus. They too, found no evidence for many of the ossifications reported by Marcus et al. (1935) that Wake and Hanken (1982) did not find in D. mexicanus, which raised further doubt about the validity of many of Marcus et al.’s observations. To clarify these conflicting observations I analyzed a nearly 42 Chapter 2 complete ontogenetic series of H. rostratus with regard to the ossifications, their homology, and their sequence of appearance. MATERIALS AND METHODS The material used in this study was collected by A. Brauer in 1896 in the Seychelles. The material is deposited in the Museum für Naturkunde, Berlin (ZMB) and also represents the source for the studies by H. Marcus and co- workers (e.g., Marcus, 1909:105, 110). I studied an ontogenetic series of embryos, juveniles and adults of Hypogeophis rostratus (Appendix). Embryos selected for clearing and staining were double stained for bone and cartilage using a slightly modified protocol based on Taylor and Van Dyke (1985). Specimens selected for serial sections were decalcified, embedded using a Shandon Hypercenter XP tissue processor, sectioned at 8 µm using a Leica SW 2000R microtome equipped with Feather N35H disposable blades and sections stained with azocarmine-red and anilin-blue (AZAN) following standard procedures (Romeis, 1989). For scanning electron microscopy (SEM), the skull of a cleared and stained juvenile was partly disarticulated and, using tweezers, the bones were gently freed from adhering fibrous tissue. Glycerin was washed out in ethanol and the bones air-dried, mounted, and sputter coated with gold-palladium. Cleared and stained specimens were observed under a Nikon SMZ-U stereomicroscope equipped with a camera lucida and a digital camera (Nikon Coolpix 995) or a Zeiss DR stereomicroscope. Photos of cleared and stained specimens were taken with a Zeiss Tessovar with a Nikon Coolpix 995 digital camera attached. Serial sections were observed under a Nikon Eclipse E600 microscope and SEM prepared specimens observed and photographed under a Hitachi S2500 SEM with a digital image capture system. The overall preservation of the material was generally very good, given the long time in storage. Some of the cleared and stained specimens did not or not completely retain the alizarin red bone stain. This was particularly the case in earlier embryos. These were observed under indirect illumination (e.g. dark
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