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Development of the Tectum in Gymnophiones, with Comparison to Other Amphibians

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Development of the Tectum in Gymnophiones, with Comparison to Other Amphibians JOURNAL OF MORPHOLOGY 236:233–246 (1998) Development of the Tectum in Gymnophiones, With Comparison to Other Amphibians ANDREA SCHMIDT1 AND MARVALEE H. WAKE2* 1University of Bremen, Brain Research Institute, 28334 Bremen, Germany 2Department of Integrative Biology and Museum of Vertebrate Zoology, University of California, Berkeley, California 94720-3140 ABSTRACT Tectal development in a number of caecilian (Gymnophiona: Amphibia) species was examined and compared with that in frogs and salamanders. The caecilian optic tectum develops along the same rostrocau- dal and lateromedial gradients as those of frogs and salamanders. However, differences exist in the time course of development. Our data suggest that, as in salamanders, simplification of morphological complexity in caecilians is due to a retardation or loss of late developmental stages. Differences in the time course of development (heterochrony) among different caecilian species are correlated with phylogenetic history as well as with variation in life histories. The most pronounced differences in development occur between the directly developing Hypogeophis rostratus and all other species examined. In this species, the increase in the degree of morphological complexity is greatly accelerated. J. Morphol. 236:233–246, 1998. ௠ 1998 Wiley-Liss, Inc. KEY WORDS: caecilian species; late developmental stages; morphological complexity The visual system of amphibians is Despite variable reduction of the visual sys- strongly correlated with phylogenetic his- tem among caecilians, the degree of morpho- tory (Roth et al., ’83, ’90; Wake, ’85; Schmidt logical complexity (lamination and number and Wake, ’91). Differences in the visual of migrated cells) in the most developed cae- system are apparent among the three orders cilian tectum is greater than in that in most of amphibians (frogs [Anura], salamanders salamanders (Schmidt and Wake, ’91, ’97), [Urodela], and caecilians [Gymnophiona]), suggesting that internal dynamics might be as well as among species within each order. more important for tectal differentiation These differences concern the absolute and than external influences. Compared with relative sizes of eyes (Wake, ’85; Roth et al., salamanders, caecilians vary especially in ’90), eye morphology (Wake, ’85; Linke et al., the localization of migrated cells. Although ’86), degree of frontal direction of the eyes salamanders possess very few migrated cells (Roth, ’87), patterns of visual projections that are present equally in both the medial (Fritzsch, ’80; Fritzsch et al., ’85; Himstedt and lateral parts of the tectum, the majority and Manteuffel, ’85; Rettig and Roth, ’86), of migrated cells in caecilians occurs in the and tectal morphology (Roth et al., ’90, ’93). lateral part of the tectum (Schmidt and The morphologically most complex optic tec- Wake, ’91, ’97). tum among amphibians is found in frogs. Many studies (e.g., Roth et al., ’93; Schmidt They possess a multiply laminated tectum and Roth, ’93) have demonstrated that differ- (Potter, ’69) in which many cells can be found ences in brain morphology are related to in the superficial neuropil. Such cells have heterochrony (i.e., dissociations or relative migrated from their periventricular origin changes in patterns of development). For during the course of development, and are known as ‘‘migrated’’ cells. This condition is in contrast to salamanders and caecilians, which have a secondarily simplified tectal Contract grant sponsor: Deutsche Forschungsgemeinschaft; morphology (Schmidt and Wake, ’91; Roth et Contract grant number: Schm 833/3-2; Contract grant sponsor: al., ’94) with a more or less homogeneous National Science Foundation. *Correspondence to: Marvalee H. Wake, Department of Integra- periventricular gray and a superficial neuro- tive Biology, 3060 VLSB, University of California, Berkeley, CA pil that exhibits very few migrated cells. 94720-3140; E-mail: [email protected] ௠ 1998 WILEY-LISS, INC. 234 A. SCHMIDT AND M.H. WAKE example, in salamanders, the simplification and Roth, ’93) by comparing the tectal devel- of the tectum mesencephali is thought to be opment in frogs with that of caecilians. Het- due to paedomorphosis characterized by a erochronies associated with differences in loss or retardation of late ontogenetic pro- life histories may be due to changes in the cesses, particularly the migration of cells action of hormones (Gilbert, ’91). For in- into the superficial neuropil (Schmidt and stance, experimental studies on skull devel- Roth, ’93). It is not known whether the low opment (Hanken and Summers, ’88a,b; Han- degree of morphological differentiation in ken and Hall, ’88) and on the development of the tectum of caecilians also is due to paedo- the nervous system (Schmidt and Bo¨ger, ’93) morphosis, or if other factors, such as the provide evidence that direct development is reduction of the peripheral visual system, due to an increase in thyroxine levels. The might contribute to the simplification. consequence is an acceleration of develop- Two major factors have been shown to be mental processes as well as a decoupling of related to interspecific variation during brain ontogenetic processes leading to the develop- development: (1) differences in genome size ment of a mosaic of characters similar to (Roth et al., ’93), and (2) differences in life those found in many direct-developing sala- histories (Rettig and Roth, ’86; Schmidt et manders. al., ’88; Wake and Roth, ’89). Both were In order to investigate the relationship shown to play an important role during brain among different life history strategies and development in salamanders (Schmidt and changes in the time course of development, Bo¨ger, ’93; Roth et al., ’93). we compared the ontogenetic sequence of In salamanders, an increase in genome tectal development in a diversity of caecilian size is thought to be correlated with the species that exhibit various life history occurrence of paedomorphosis, in that it modes. leads to a general slowing down of develop- MATERIALS AND METHODS ment (Wake, ’66; Cavalier-Smith, ’78; Hor- Species and stages examined ner and MacGregor, ’83; Sessions and Lar- Tectal development was studied in five son, ’87; Roth et al., ’93, ’94). Frogs possess species of three of the six families of the smaller genomes than salamanders (Olmo, Order Gymnophiona (Duellman and Trueb, ’83). The genome sizes of caecilians lie be- ’86; Nussbaum and Wilkinson, ’89; Hedges tween those of frogs and salamanders (M.H. et al., ’93); we currently accept Typhlonecti- Wake and S.K. Sessions, unpublished obser- dae as a distinct family, as do most research- vations). Presuming that there is a relation- ers on caecilian biology) that have differ- ship between an increase in genome size and ent life history strategies. Families and the degree of paedomorphosis, one would species include Ichthyophidae: Ichthyophis expect that paedomorphosis does not affect kohtaoensis (Southeast Asia [Thailand]; brain development as strongly in caecilians oviparous); Caeciliidae: Dermophis mexica- as it does in salamanders. nus and Gymnopis multiplicata (both Cen- Roth et al. (’93) presented a phylogenetic tral America [Mexico to Panama and Costa analysis of the evolution of the brain in Rica, respectively]; both viviparous); Hypo- vertebrates, using 23 neuroanatomical char- geophis rostratus (Seychelle Islands; direct acters, including those of the tectum. Their development); and Typhlonectes compressi- most parsimonious conclusion is that a com- caudus (South America [north-central]; vi- plex brain is the ancestral condition, and viparous). Most animals were collected, dis- secondary simplification occurred indepen- patched, and preserved immediately in the dently in hagfishes, lepidosirenid lungfishes, field. and salamanders and caecilians. Therefore, Tectal development was studied in the assuming that frogs possess the ancestral heads of animals at different ontogenetic condition of adult tectal morphology and of stages. Parameters for choosing stages were tectal development, and given the informa- (1) presumed time past fertilization, and tion about the ontogenetic sequence of tectal (2) size (total length [TL]): Ichthyophis development in frogs (Schmidt and Roth, kohtaoensis (newly hatched larva/66 mm); ’93), we have a means of evaluating whether Dermophis mexicanus (1.5 months/20 mm, 2 differences in the degree of morphological months/37 mm, 2.5 months/40 mm, 3 complexity in caecilians are also due to months/49 mm, 5 months/79 mm); Gymno- changes in the time course of development, pis multiplicata (2 months/30 mm, 3 as has been shown in salamanders (Schmidt months/54 mm, 5 months/84 mm); Typhlo- CAECILIAN TECTAL DEVELOPMENT 235 nectes compressicaudus (approximately 3 somewhat more intense in the medial than months/46 mm); Hypogeophis rostratus (age in the lateral zone. The superficial neuropil undeterminable/38 mm). begins to develop, and the first migrated cells appear. The lateral part of the tectum is Methods always the first part in which a superficial Specimens were fixed in 10% neutral buff- neuropil and migrated cells are found, and ered formalin for a minimum of 72 hr and the region where, compared with the medial preserved in 70% ethanol. Heads were re- zone, cell proliferation increases initially and moved, decalcified in 3% formic acid, embed- then also decreases first. From stage 30 (in ded in paraffin, and transversely sectioned the rostral tectum) and stage 37 (in the at 10 µm. Every third slide was stained with caudal tectum), the
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