Cellular Migration and Morphological Complexity in the Caecilian Brain

JOURNAL OF MORPHOLOGY 231:11–28 (1997) Cellular Migration and Morphological Complexity in the Caecilian Brain ANDREA SCHMIDT1 AND MARVALEE H. WAKE2* 1Brain Research Institute, University of Bremen, 28334 Bremen, Germany 2Department of Integrative Biology and Museum of Vertebrate Zoology, University of California, Berkeley, California 94720 ABSTRACT The morphology of the tectum mesencephali and the medial pallium is studied in species representing the six families of caecilians (Amphibia: Gymnophiona) in order to determine whether differences in brain morphology are related to function, phylogenetic history, or life history strategies. In general, the caecilian tectum is characterized by simplification in having little to no lamination and few migrated cells. The degree of morphological complexity differs between species and between brain regions. Our data suggest that changes in brain morphology are due to a mosaic of different influences. We did not find a strict correlation between visual system reduction and tectal morphologies. However, phylogenetic effects exist. The greatest degree of morphological complexity is found in members of the Rhinatrema- tidae, a family that is considered basal to the lineage. Thus, simplification of brain morphology in caecilians must be considered a secondary or derived rather than a primitive feature. Direct development and miniaturization are correlated with the greatest simplification in the tectum mesencephali and medial pallium. There is a relationship between differences in brain morphology and heterochrony in caecilians, as in other amphibians. J. Morphol. 231:11–27, 1997. r 1997 Wiley-Liss, Inc. The morphology of the brain of members layer and a superficial fiber layer containing of the three modern orders of amphibians— very few migrated cells (Roth et al., ’90b; frogs (Anura), salamanders (Caudata) and Schmidt and Wake, ’91). In salamanders, caecilians (Gymnophiona)—differs not only not only the tectum mesencephali but also in the relative sizes of different brain re- other regions are affected by the reduction of gions but also in the degree of morphological cell migration (Roth et al., ’93; Wake et al., complexity of the parts. The caecilian brain ’88). Only the medial pallium always shows is characterized by a large telencephalon, cell migration (Roth et al., ’93). In the past, and a very small tectum mesencephali, an simple morphology was interpreted to be a important area for sensory integration that primitive (Herrick, ’48; Leghissa, ’62) and receives primary visual projections. Small unspecialized state. However, a recent phy- size is in concordance with the reduction of logenetic analysis suggests that simple mor- the visual system in these animals (Man- phology is an apomorphic trait and due to teuffel and Himstedt, ’85; Wake, ’85). The secondary, derived simplification (Roth et tectum mesencephali also differs between al., ’92, ’93). frogs and salamanders. The tectum of an- Major factors that trigger brain morpho- urans is large, expanded, and multiply lami- genesis are 1) stimulation by afferents and nated (Fig. 2a). It consists of nine alternat- 2) changes in the time course of development ing cellular and fiber layers (Potter, ’69). The (Finlay et al., ’87; Roth et al., ’93; Schmidt superficial fiber layers (layers 7–9) contain a and Roth, ’93). Caecilians are characterized substantial number of migrated cells (up to by a reduction of the entire visual system. 30%). These layers resemble the tectum of The degree of reduction differs interspecifi- most other groups of vertebrates (Vanegas et cally (Wake, ’85). It is currently not known al., ’84). In contrast, the tectum of salamanders and caecilians (Fig. 2b,c) is very *Correspondence to: M.H. Wake, Department of Integrative simple. It has only a periventricular cellular Biology, University of California, Berkeley, CA 94720-3140. r 1997 WILEY-LISS, INC. 12 A. SCHMIDT AND M.H. WAKE Fig. 1. Cladogram illustrating currently accepted hypothesis of relationships of families of caecilians (Order Gymnophiona). Species examined in this study are listed below the family name. whether or how the reduction of the visual ’78). The genome sizes of caecilians (Ses- periphery affects the morphological complex- sions and Wake, unpublished) lie between ity of the tectum and what secondary effects those of salamanders, which are character- on the development of other brain regions ized by large genomes and a very simple might arise. Is, for example, the expansion tectal morphology (Roth et al., ’90a, ’93), and of the telencephalon and the elaborated olfac- those of frogs, which have small genomes tory system (Schmidt and Wake, ’90) in these and a multiply laminated tectum. Changes animals indirectly related to the reduction in the time course of development also occur of the visual system? in the context of differences in life history In urodeles, simplified brain morphology strategies. For example, some frogs and sala- is considered to be due to a change in the manders that have direct development (fer- time course of development, in the sense tilized eggs laid on land, development that late ontogenetic stages are retarded or through metamorphosis before hatching so lost (Roth et al., ’93; Schmidt and Roth, ’93). that a free-living larval period does not oc- In consequence adult animals retain juve- cur) are characterized by an acceleration or nile characters in the adult stage and are condensation of early ontogenetic stages. The thus considered paedomorphic. The retarda- more common and presumably plesiomor- tion of development in these animals is phic life history mode is shown by species thought to be due to a decrease in rates of that lay eggs that develop into larvae, char- cell metabolism and cell proliferation that is acterized by a suite of characters involving a correlated with an increase in genome and free-living aquatic period before a relatively cell size (Sessions and Larson, ’87; Roth et profound metamorphosis into the juvenile/ al., ’90a; Szarski, ’76, ’83; Cavalier-Smith, adult form. Among salamanders the most CAECILIAN BRAIN 13 simplified brains in terms of degree of lami- (West Africa, both viviparous) (see Table 1 nation and cellular migration occur in minia- for reproductive modes). turized, direct developing, derived species (Roth et al., ’90a, ’94). Methods The gymnophione amphibians show a di- versity of structure-function modifications The morphology of the tectum was exam- and life history patterns that is not seen in ined in heads of adult specimens, obtained other amphibians, at least to the same ex- from numerous individuals, museums, and tent. These features include limblessness, collections (see Wake, ’86, ’92). Material was visual reduction, and viviparity (retention of formalin-fixed and preserved in 70% etha- embryos with maternal nutrition following nol. Heads were removed, decalcified, and resorption of yolk, and birth of fully meta- embedded in paraffin and serially sectioned morphosed young). In order to determine (transversely or horizontally) at 7–10 µm. whether differences in brain morphology are Every third slide was stained with picro- related to function and/or phylogenetic ponceau, hematoxylin-eosin, or Mallory’s history and/or life history strategies, we in- azan according to standard procedures (Hu- vestigated the morphology of the tectum mes- manson, ’79). Since an exact identification of encephali and the medial pallium of repre- tectal borders can be made only from trans- sentative species of the six families of caecilians, verse sections, only those species for which which differ in both the degree of reduction we had such sections were studied quantita- of the visual system and in life history strat- tively (E. bicolor (N 5 2), D. mexicanus egies. (N 5 3), T. natans (N 5 1), B. boulengeri (N 5 1), and S. uluguruensis [N 5 1]). Every MATERIALS AND METHODS third section was drawn with the aid of a Species examined camera lucida. From these drawings we de- Tectal morphology was studied in repre- termined total cell number and number of sentatives of all six families of the Order migrated cells in the superficial fiber layer Gymnophiona (Fig. 1) (see Duellman and and calculated the percentage of white mat- Trueb, ’86; Nussbaum and Wilkinson, ’89; ter. Areas (i.e., the periventricular cellular but also see Hedges et al., ’93). Families and layer and the white matter) were measured species studied include Rhinatrematidae using a graphic tablet (Summagraphics, Aus- (northern South America), Epicrionops pe- tin, TX) and its program. Each migrated cell tersi and Epicrionops bicolor (both with an was counted. In order to approximate the aquatic larval stage); Ichthyophiidae (south- genome size, we determined the nuclear size east Asia), Ichthyophis kohtaoensis (aquatic by calculating the mean diameter of nuclei larval stage); Uraeotyphlidae (India), Uraeo- of eight to twelve cells/section, ten sections typhlus narayani (aquatic larval stage in- per specimen (genome size is highly corre- ferred from condition of congener [Wilkin- lated with nuclear and cell size; see Discus- son, ’92]); Caeciliidae (Central and South sion and Table 1). Tables 2 and 3 present America, Africa, Seychelles, India), Caecilia analyses of comparative organization of the occidentalis (Peru, life history not known), tectum, telencephalon, and the visual sys- Dermophis mexicanus (Central America, vi- tem, emphasizing degrees of differentiation, viparous), Gymnopis multiplicata (Central complexity, and cell migration for

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