JOURNAL OF MORPHOLOGY 236:233–246 (1998)

Development of the Tectum in Gymnophiones, With Comparison to Other

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 (: 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 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 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 zone of medial cell prolif- picroponceau (for connective tissue; nuclei of eration decreases. Lamination starts at stage brain cells were particularly well stained) 28 in the rostral tectum and at stage 37 in hematoxylin and eosin (H&E) (for contrast), the caudal tectum. or Mallory’s azan (for tissue distinctivity) according to standard procedures (Huma- Pleurodeles waltl son, ’79). Other series were stained with As in Rana temporaria, the tectum of the Palmgren’s silver specifically to display neu- salamander Pleurodeles waltl develops along ron morphology. In sections stained using rostrocaudal and lateromedial gradients. The these methods, regions of notable cell prolif- mode of cellular proliferation is similar to eration can be distinguished from those with that of Rana temporaria. However, in gen- no or low proliferation by dark staining of eral, cell proliferation in Pleurodeles is less nuclei and the appearance of elongated neu- extensive than in Rana temporaria. This rons in addition to compact cells. becomes most obvious at midlarval and late ontogenetic stages. At early stages (33–37 RESULTS [staging according to Gallien and Durocher, Tectal development in frogs ’57], in the rostral tectum), cell proliferation and salamanders occurs all over the entire width of the epen- The anuran tectum is a conspicuously mul- dymal layer, with a slight concentration in tilayered structure that is divided into nine the lateral part of the tectum (Fig. 1B). The alternating cellular and fiber layers (Potter, superficial neuropil begins to develop at stage ’69). Many migrated cells (Յ30%) are found 34. The small numbers of migrated cells do in the superficial fiber layer. By contrast, the not appear before stage 36. The tectum of salamander tectum is characterized by a Pleurodeles exhibits no distinct multiple thick periventricular cellular layer and an lamination. Starting at stage 38, cell prolif- outer fiber layer that contains only few mi- eration decreases, beginning in the rostral grated cells (Roth et al., ’93). tectum. At this time there is a stronger cell proliferation in the medial than in the lat- Rana temporaria eral zone of the tectum. Cell proliferation in The optic tectum of the frog Rana tempo- the lateral zone is minimal and also de- raria develops along rostrocaudal and latero- creases in the medial zone, starting in the medial gradients. The lateral part of the rostral tectum at stage 42. At this stage, rostral tectum differentiates first and the Pleurodeles is only 20% throughout its lar- medial part of the caudal tectum differenti- val period. ates last (Schmidt and Roth, ’93). At early stage 24 (Gosner, ’60), cell proliferation takes Tectal development in caecilians place over the entire width of the ependymal The caecilian tectum, like that of sala- layer, more strongly laterally than medially manders, appears rather simple and con- (Fig. 1A). A superficial neuropil is absent. sists primarily of a periventricular cellular This mode of cellular proliferation is found layer and a superficial fiber layer, that, how- over all the tectum (rostral, central and me- ever, contains relatively more migrated cells dial). From stage 25 (in the rostral tectum) than salamanders. In caecilians, migrated and stage 31 (in the caudal tectum), cell cells occur primarily in the lateral part of proliferation occurs in both a medial and in a the tectum rather than in the medial part. lateral zone, with an intermediate zone of Among caecilians, there are differences in low cell proliferation lying between these the complexity of the cellular layer, as well zones. At this time, cellular proliferation is as in the number of migrated cells (Schmidt 236 A. SCHMIDT AND M.H. WAKE

Fig. 1. Sequence of tectal development in the frog rows) occurs all over the tectum during early stages Rana temporaria (A,C,E) and the salamander Pleurode- (A,B) and is restricted to a lateral and medial zone at les waltl (B,D,F). Transverse sections of the central later stages (C,D). Cell proliferation in Pleurodeles is tectum. A,B: Early stages, shortly after hatching. C,D: less than in Rana and stops earlier in relative to the Midlarval stages. E,F: Shortly before metamorphosis. time of metamorphosis. Bar ϭ 100 µm. In both species, cell proliferation (ar- and Wake, ’97). In some species (e.g., Gymno- nectes, and Ichthyophis possess a moderate pis multiplicata), the periventricular cellu- degree of morphological complexity and a lar layer is homogeneous, whereas in other moderate number of migrated cells within species (e.g., Dermophis mexicanus, Ichthyo- the superficial neuropil. Gymnopis and Der- phis kohtaoensis, Hypogeophis rostratus, and mophis both possess many migrated cells. Typhlonectes compressicandus), it is tra- However, in contrast to Gymnopis, which versed by fibers that in most cases do not has a homogeneous cellular layer, Dermo- constitute continuous layers. Among the cae- phis has the most complex tectum among cilian taxa examined, Hypogeophis, Typhlo- the genera examined. CAECILIAN TECTAL DEVELOPMENT 237 In all the caecilian species examined, the cells are found in the lateral part. The cau- ontogenetic sequence of cellular prolifera- dal tectum does not have any migrated cells. tion and cellular migration is basically the The superficial neuropil is best developed in same as that described for frogs. However, the rostral tectum and diminishes caudad. there are changes in the time course of devel- The caudalmost tectum has only a small opment and in the intensity of cell prolifera- amount of neuropil in both the lateral and tion. As in Rana, cell proliferation takes the medial areas (Fig. 2F). place over all the ependymal layer early in 79-mm TL. The rostral and the central development, with a concentration in the tectum lack zones of cellular proliferation. lateral part of the tectum (Figs. 2, 3, 6). At An extensive cell proliferation is found only later developmental stages the rate of lat- in the caudal tectum where it is concen- eral cell proliferation decreases. In contrast trated laterally. Migrated cells are found in to Rana, there is no increase in cell prolifera- the rostral as well as in the central and the tion in the medial zone. Tectal development caudal tectum, but they are mainly re- in caecilians also proceeds along rostrocau- stricted to the lateral tectum. Very few mi- dal and lateromedial gradients. The lateral grated cells occur in the medial tectum. The part of the rostral tectum is the first part in superficial neuropil is most developed in the which a superficial neuropil and migrated rostral and central portions of the tectum, cells are found; the medial part of the caudal but a lesser amount of neuropil is present in tectum is the region in which these pro- the caudal tectum, where it is better devel- cesses occur last. oped in the lateral than in the medial part. Dermophis mexicanus Gymnopis multiplicata 20-mm TL. Cell proliferation occurs over 30-mm TL. At this stage, tectal morphol- the entire width of the ependymal layer in ogy is similar to that of the 37-mm specimen the rostral, central, and caudal tectum (Fig. of Dermophis. There is little cell prolifera- 2A,C,E). A small amount of superficial neuro- tion in the rostral tectum (Fig. 3A), but it pil that diminishes rostrocaudally is found occurs equally in the medial and the lateral in the lateral tectum. There are no migrated zones. Extensive cell proliferation occurs lat- cells. erally and to a lesser degree medially within 37-mm TL. Cell proliferation is concen- the central tectum (Fig. 3C). Cell prolifera- trated in the lateral tectum. It is least in the tion increases caudad, and is greater in the rostral tectum and most extensive in the lateral than in the medial zone (Fig. 3E). caudal tectum. Compared with the 20-mm Very few migrated cells are apparent in the individual, cell proliferation in the 37-mm rostral and central tectum, and none is found TL is decreased medially in all parts in the caudalmost tectum. The superficial of the tectum. In the rostral and in the neuropil is best developed in the lateral part central tectum, a few migrated cells occur in of the rostral tectum and diminishes caudo- the ventralmost part of the lateral tectum. medially. Substantial numbers of migrated cells are 54-mm TL. At this stage, there is little to found in the adjacent thalamic and tegmen- no cellular proliferation in the rostral and tal areas. No migrated cells are found in the central tectum (Fig. 3B,D). Extensive prolif- caudalmost part of the tectum. The superfi- eration occurs in the lateral zone of the cial neuropil is present in the lateral tectum, caudal tectum (Fig. 3F), and less prolifera- but there is very little neuropil in the medial tion occurs in the medial zone. Few migrated tectum. The amount of superficial neuropil cells are found in the rostral tectum. More diminishes rostrocaudally. migrated cells are found in the central tec- 49-mm TL. The rostral tectum lacks dis- tum and especially in the adjacent tegmen- tinctive zones of cellular proliferation (Fig. tum. There are still no migrated cells in the 2B). In the central tectum, cell proliferation caudalmost tectum. The superficial neuropil is restricted to a lateral zone (Fig. 2D). There is best developed in the lateral part of the is no cell proliferation in the medial zone. rostral tectum and diminishes caudomedi- The caudal tectum (Fig. 2F) exhibits an ex- ally. tensive cell proliferation that is concen- 84-mm TL. Cellular proliferation is com- trated in the lateral zone. Less cell prolifera- pleted in the rostral, central, and caudal tion occurs in the medial tectum. In the tectum. In all parts of the tectum (rostral, rostral and central tectum, few migrated central and caudal), the superficial neuropil 238 A. SCHMIDT AND M.H. WAKE

Fig. 2. Sequence of tectal development in Dermophis caudal (C) tectum. In the 49-mm animal, this early mexicanus (viviparous). A,C,E: 20-mm animal. B,D,F: pattern of cell proliferation only occurs in the caudal 49-mm animal. Transverse sections of the rostral (A,B), tectum. In the central tectum, cell proliferation is re- central (C,D), and caudal (E,F) tectum. In the 20-mm stricted to a lateral zone. Proliferation already stopped animal, cell proliferation (arrows) occurs all over the in the rostral tectum. Bar ϭ 100 µm. ependymal layer in the rostral (A), central (B), and is well developed, and a substantial number tion occurs over the entire width of the epen- of migrated cells appear in the lateral part of dymal layer (Fig. 4C). No difference in prolif- the tectum. Very few migrated cells are ap- erative activity is found between the lateral parent in the medial part of the tectum. and medial tectum as described in Gymno- pis and Dermophis. There are very few mi- Typhlonectes compressicaudus grated cells in the lateral part of the rostral 46-mm TL. Compared with other taxa, tectum (Fig. 4A). Compared with Dermophis tectal cell proliferation in Typhlonectes is and Gymnopis at similar sizes, the relative much reduced. Hardly any proliferative size of the neuropil is very small. Also in zones can be distinguished except in the Typhlonectes, the neuropil is more developed caudal tectum (Fig. 4E), where cell prolifera- in the rostral than in the caudal tectum. CAECILIAN TECTAL DEVELOPMENT 239

Fig. 3. Sequence of tectal development in Gymnopis pattern of cell proliferation (cell proliferation all over multiplicata (viviparous). A,C,E: 30-mm animal. B,D,F: the ependymal layer; arrows). In the central (C) tectum, 54-mm animal. Transverse sections of the rostral (A,B), proliferation is restricted to a lateral zone. In the rostral central (C,D), and caudal (E,F) tectum. In the 30-mm tectum (A), cell proliferation is highly reduced. In the animal, cell proliferation (arrows) occurs in all parts of 54-mm animal, cell proliferation only occurs in the cau- the tectum, but only the caudal tectum shows the early dal tectum (arrows). Bar ϭ 100 µm.

Hypogeophis rostratus medial part. The superficial neuropil is well 38-mm TL. At this stage, tectal develop- developed in the rostral, central, and caudal ment is nearly complete. Neither rostral (Fig. tectum. 4B), central (Fig. 4D), nor caudal tectum (Fig. 4F) possesses distinctive zones of cellu- Ichthyophis kohtaoensis lar proliferation. The number of migrated 66-mm TL. At this stage, tectal develop- cells is very low within the rostral tectum ment is well advanced. No distinctive zones but increases caudad. Most migrated cells are found in the rostral, central, and caudal are concentrated in the lateral tectum and tectum (Fig. 5). A few migrated cells occur in adjacent tegmentum. Very few occur in the the rostral, central and caudal tectum. These 240 A. SCHMIDT AND M.H. WAKE

Fig. 4. A,C,E: 46-mm Typhlonectes compressicaudus zones can be distinguished, except in the caudal tectum (viviparous). B,D,F: 38-mm Hypogeophis rostratus (di- (arrows). In Hypogeophis, tectal development already is rect development). Transverse sections of rostral (A,B), nearly completed in the 38-mm animal. At this stage, central (C,D), and caudal (E,F) tectum. In Typhlonectes, there are no distinctive zones of cell proliferation. Bar ϭ cell proliferation is very low. Hardly any proliferative 100 µm. are concentrated in the lateral tectum. More ever, there are differences in the time course migrated cells are found in the thalamus of development regarding cellular prolifera- and tegmentum. tion and the degree of cellular migration. Differences in the time course of tectal devel- DISCUSSION opment exist not only between frogs and Our examination shows that the caecilian salamanders, but also among caecilian spe- tectum develops along the same rostrocau- cies. Our results suggest that interspecific dal and lateromedial gradients (Straznicky differences in tectal development are related and Gaze, ’72; Schmidt and Roth, ’93) as to differences in life histories among caecil- those of frogs and salamanders (Fig. 6). How- ian taxa. CAECILIAN TECTAL DEVELOPMENT 241 features into the adult stage, thus, the adult morphology is paedomorphic. Our results suggest that the simplification of tectal mor- phology in caecilians is also due to paedomor- phosis. However, tectal development in cae- cilians is not as strongly affected by paedomorphosis as is tectal development in salamanders. In caecilians, cellular proliferation occurs all over the tectum at early ontogenetic stages but concentrates in the caudal tectum at late stages. In frogs, the homogeneous layer of extensive cell proliferation splits off during development, so that at later stages cell proliferation occurs in distinct medial and lateral proliferative zones (Figs. 1, 6). These two zones differ in degree of cellular proliferation. The lateral zone exhibits most extensive cell proliferation at early ontoge- netic stages but, in this zone, cell prolifera- tion also decreases earlier than in the me- dial zone. In the medial zone, the peak of proliferative activity is found at later devel- opmental stages and the decrease in cell proliferation occurs later than in the lateral zone. This sequence of tectal development is concordant with that described in other ver- tebrates, such as trout (Richter, ’81; Man- sour-Robaey and Pinganaud, ’90). In sala- manders, simplification of tectal morphology is due to a decrease in cell proliferation both in the lateral zone and in the medial zone (Schmidt and Roth, ’93). Cell proliferation in salamanders is suppressed during late as well as during early developmental stages (Fig. 6). Caecilians differ from frogs but are similar to salamanders in that, in general, the medial zone shows very low proliferative activity that never increases (Fig. 6), but it decreases early in development. Consequently, Fig. 5. 66-mm Ichthyophis kohtaoensis (biphasic de- the late-occurring mode of cell proliferation is velopment). Transverse sections of the rostral (A), cen- delayed in caecilians. By contrast, the pattern tral (B), and caudal (C) tectum. Tectal development is of early cellular proliferation is similar to that well advanced. Distinctive zones of proliferative activity have disappeared. Bar ϭ 100 µm. of frogs but differs from that of salamanders. In caecilians, extensive cell proliferation within the lateral zone occurs early and persists until mid-developmental stages (Fig. 6). This Is the simplification of the tectum in is in contrast to salamanders, in which cell caecilians due to heterochrony? proliferation in the lateral zone is greatly It is well known that heterochrony plays reduced. Differences in patterns of cellular an important role in creating phylogenetic proliferation between salamanders and cae- change (Wake, ’66; Gould, ’77; Alberch, ’80, cilians are concordant with differences in ’82). Comparative studies of frogs and sala- the distribution of migrated cells at the adult manders provide evidence that the simpli- stage. In the adult salamander tectum, there fied brain morphology in salamanders repre- are very few migrated cells in the medial sents the retention of early ontogenetic and in the lateral tectum. In contrast to 242 A. SCHMIDT AND M.H. WAKE

Fig. 6. Schematic drawing of ontogenetic changes in developmental stages, cell proliferation is restricted to the mode of cell proliferation in anurans, urodeles, and lateral and medial edges of the tectum. Compared with caecilians. Black regions, areas of strong cell prolifera- the situation in frogs, cell proliferation in salamanders tion; dotted regions, areas of low cell proliferation. A: and caecilians is highly reduced. In salamanders, the Proliferation during early ontogenetic stages. B: Prolif- reduction especially affects the lateral zone. In caecil- eration during mid-developmental stages. C: Prolifera- ians strong cell proliferation persists in the lateral zone tion during metamorphic stages. D: Distribution of mi- but is highly reduced in the medial zone. Differences in grated cells in the adult tectum of the three proliferative activity among the three amphibian orders orders. In all three orders, cell proliferation occurs all correlate with differences in the distribution of migrated over the ependymal layer at early stages. At mid- cells within the adult tectum (D). salamanders, migrated cells in the caecilian early as well as at late stages, only late tectum, although few in number, are concen- stages are retarded in caecilians. Thus, cae- trated mainly in the lateral tectum (Schmidt cilians are not as strongly affected by paedo- and Wake, ’91). morphosis as are salamanders. In summary, our data suggest that simpli- fication of morphological complexity in the Relationship between heterochronic optic tectum of caecilians is due to a retarda- development of the tectum and differences tion or loss of late developmental stages. in life histories However, in contrast to salamanders, which Heterochrony affecting the tectum occurs show retardation of tectal development at in all the three amphibian orders and among CAECILIAN TECTAL DEVELOPMENT 243 species of caecilians. While the general ros- to direct development. This finding is concor- trocaudal and lateromedial sequence of tec- dant with the situation in salamanders tal development is the same, the time course where characteristics in the morphology of differs among caecilians. Our data suggest the feeding apparatus and the visual system that differences in tectal development are at in members of the tribe Bolitoglossini (Fam- least partially correlated with differences in ily Plethodontidae) are attributed to an onto- life histories. However, the fact that varia- genetic repatterning related to direct devel- tion in tectum developmental patterns also opment (Wake and Roth, ’89). Studies on occurs among caecilian species that possess Pleurodeles waltl, a salamandrid with an the same life history suggests that heteroch- aquatic larval stage, demonstrate that an ronies are correlated with phylogenetic his- ontogenetic repatterning similar to that of tories as well. direct-developing bolitoglossine salamanders In order to compare patterns of heteroch- can be induced by increasing thyroxine dur- rony, criteria for the evaluation of the stage ing early developmental stages (Schmidt and of tectal development must be established. Bo¨ger, ’93). Changes due to thyroxine in- Our criteria include the following: (1) the clude an acceleration of the rostro-caudal degree of cellular migration, (2) the size of sequence of tectal development. The relation- the superficial neuropil, and (3) the morpho- ship among differences in life history, differ- logical complexity of the periventricular cel- ences in the action of hormones, and neuro- lular layer. During development, these pa- nal development needs investigation in rameters differ among the rostral, central, caecilians. Caecilians provide an unusual and caudal tectum. The rostral tectum differ- paradigm for examination of the association entiates earliest and the caudal tectum dif- of hormones and life history strategies. ferentiates last. Therefore a comparison of Oviparous caecilians with free-living larvae the above-mentioned criteria among the ros- typically have long larval periods (e.g., Ich- tral, central, and caudal tectum makes it thyophis glutinosus [Breckenridge and Jay- possible to evaluate whether development is asinghe, ’79; Breckenridge et al., ’87], but completed or whether it has just begun. A perhaps not Sylvacaecilia grandisonae [Lar- well-differentiated caudal tectum indicates gen et al., ’72]). they thus have a lengthy that development is already completed. In period of development dependent on endog- contrast, an undifferentiated rostral tectum enous hormones. Direct-developing animals represents an early developmental stage. presumably have a different interaction of Marked differences in tectal development maternal and embryonic hormones, as sug- occur between the direct-developing caecil- gested by studies in frogs (Jennings and ian Hypogeophis and all other taxa exam- Hanken, ’94) and salamanders (Schmidt and ined. Our results show that in a 38-mm Bo¨ger, ’93). The protracted gestation period prehatching (15% of average adult length) in viviparous caecilians, with its dissocia- Hypogeophis embryo, tectal development is tion of many developmental, especially far advanced. Cell migration has occurred ‘‘metamorphic’’ events, is probably the result all over the tectum with a concentration in of a complex interaction of fetal and mater- the lateral part of tectum. In particular, the nal hormones (Wake, ’89, ’94). Among the late-developing caudal tectum possesses taxa examined, Typhlonectes, a viviparous many migrated cells. Also, a superficial neu- genus, is characterized by the slowest devel- ropil has already developed in this region. opment that especially affects the develop- Tectal morphology in a 38-mm Hypogeophis ment of the neuropil and cell migration embryo resembles that found in a newly (based on a 46-mm fetus, 10% of total aver- hatched larva of Ichthyophis at a length of age adult length, with fetal size represent- 66 mm (25% of total average adult length). ing sample size, not fetal maximum). We Thus, these species exhibit a dissociation of find few migrated cells, and there is little development of body size and tectal develop- neuropil in all parts of the brain. However, ment. In the viviparous caecilians Gymnopis relative to the development of the neuropil, multiplicata and Dermophis mexicanus, a the rostrocaudal retraction of proliferation developmental stage of tectal development zones is advanced and corresponds to that similar to the 38-mm Hypogeophis is not found in Dermophis (fetus 49 mm, 15% of achieved until the animal reaches lengths of average adult total length) and Gymnopis about 84 mm and 79 mm, respectively. The (54 mm, 15% of average adult total length). dissociation between body growth and tectal There are also differences concerning the development in Hypogeophis suggests an on- distinction of proliferation zones. In Typhlo- togenetic repatterning that may be related nectes, no distinctive zones of cellular prolif- 244 A. SCHMIDT AND M.H. WAKE eration can be distinguished except in the related to direct development (Schmidt and caudal tectum. Differences among vivipa- Bo¨ger, ’93). The fact that the degree of mor- rous species might be due to phylogenetic phological complexity of the tectum in Typh- relationships. Closely related genera, such lonectes is similar to that in Hypogeophis as Gymnopis and Dermophis, have the great- indicates that despite a slower rate of devel- est similarities concerning the time course opment, a similar degree of morphological of tectal development. There are very few complexity can be achieved. Further investi- differences in the relationship between gation is needed to show whether this is due growth rate (in terms of body size) and tectal to an extension of developmental time. development in these genera. A comparison of Hypogeophis with Gymno- How do changes in the time course of tectal pis and Dermophis shows that, despite an development in caecilians affect adult early delay in development in Gymnopis and morphology? Dermophis, there are more migrated cells in A comparison of differences in the time adults of these two genera, which may be course of tectal development with the degree due to their extensive cell proliferation. The of adult morphological complexity shows that superficial neuropil increases concomitantly. different taxa may have similar adult tectal Even though these processes occur rela- morphologies but may vary in the time tively later during ontogeny, in comparison course of development (e.g., Ichthyophis, to Hypogeophis, they overcompensate for the Typhlonectes, and Hypogeophis). Adults of early delay in development in Gymnopis and these species possess a moderate number of Dermophis. migrated cells and a moderate degree of However, in contrast to Gymnopis and Der- morphological complexity within the periven- mophis, cell proliferation in the tectum of tricular gray (Schmidt and Wake, ’97). De- the 46-mm Typhlonectes, another viviparous spite these similarities, the time course of species in a different family, is limited and development varies. In Hypogeophis, tectal development occurs quickly during early de- the superficial neuropil is relatively small. velopmental stages, whereas tectal develop- Typhlonectes possesses a moderate number ment proceeds slowly in Typhlonectes. The of migrated cells during adulthood. Such most parsimonious prediction is that an ani- differences illustrate the correlation with mal characterized by rapid development phylogenetic history, which may be dis- should have the greatest degree of morpho- tinctly different with regard to developmen- logical complexity as an adult, and an ani- tal patterns in taxa with the same reproduc- mal that develops slowly would have a lesser tive modes. degree of morphological complexity as an In summary, our data show that phyloge- adult. However, similarities in the degree of netic history correlates with similarities in morphological complexity between Typhlo- the time course of tectal development and nectes and Hypogeophis suggest a more com- thus leads to a similar morphological com- plex scenario. The degree of morphological plexity in the adult brain. However, similari- complexity not only depends on the rate of ties in morphological complexity do not nec- development, but also on the end-point of essarily predict a similar time course of development or the onset of a slowdown in development. Alternatively, a similar degree development. If the latter occurs early, the of morphological complexity can be achieved effects of a previous acceleration might be as a result of variation in the onset and compensated. This may be the case in Hypo- course of developmental processes (cell pro- geophis, and it may be related to direct devel- liferation, development of the neuropil). The opment. Similar changes in developmental rates were demonstrated in the salamander critical period is presumably the end of devel- Pleurodeles waltl after hormonal treatments opment (larval, direct-developing embry- (Schmidt and Bo¨ger, ’93). These studies show onic, or fetal) or the time when a general that an increase in thyroxine during early slowdown occurs. Our data suggest that het- developmental stages leads to an accelera- erochrony in caecilians is related to varia- tion of development. However, due to a short- tion in life history strategies. Further inves- ening of the larval stage, these animals re- tigation is needed to clarify the significance tain early ontogenetic characters. In of variation in life histories and differences salamanders, these effects, which are in- in the hormonal control involved in the regu- duced by thyroxine, are considered to be lation of development in amphibians. CAECILIAN TECTAL DEVELOPMENT 245

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