Fetal tooth development and adult replacement in Dermophis ...

JOURNAL OF MORPHOLOGY 166203-216 (1980)

Fetal Tooth Development and Adult Replacement in Dermophis mexicanus (Amphibia: Gymnophiona): Fields Versus Clones

MARVALEE H. WAKE Department of Zoology and Museum of Vertebrate Zoology, University of California, Berkeley, California 94720

ABSTRACT Teeth of fetuses of a caecilian, Dermophis mexicanus (Amphibia: Gymnophiona), show ontogenetic variation in crown structure from small, multidenticulate, and non-pedicellate to larger, spoon-shaped, pedicellate teeth with a single apical spike. Number of denticles decreases as enamel-secreting cells mature. Numbers of teeth and of tooth rows increase ontogenetically. A fetal vomeropalatine set of teeth is present in D. mexicanus but absent in species previously examined. Teeth transitional to the adult shape and arrangement appear shortly before birth. The transition is correlated with birth, not fetal size. There is relatively little increase in numbers of teeth during the juvenile period. The pattern of development does not fully agree with either morphogenetic field theory or with clone theory, both as defined by Osborn (‘78). Sequence of initiation is appropriate to either. Tooth shape changes agree with aspects of clone theory. Multiple rows of fetal teeth and the transition to adult follow field theory. Clone theory holds that patterns of development and shape are self- regulated, field theory that they are controlled extrinsically. I suggest that substances regulating differentiation mediate early development, and hormones later development, including inception of adult teeth, and are comparable to “field substances” influencing primordia that originate according to clone theory. Components of both theories are appropriate to analyzing tooth development phenomena.

Recently attention has been paid to the considerable species-specific and ontogenetic variation in fetal and adult dentitions of caecilians (Amphibia: Gymnophiona). Fetal tooth crown morphology and tooth position are mod- ified extensively during the abrupt transition from fetal state to adult; this change, and some adult variation, are correlated with mode of feeding. Parker (’56) and Parker and Dunn (’64) considered the teeth non-adaptive, non-functional vestiges of a piscine ancestry; Wake (’76, ’77a,b, ’78) emphasized the functional nature of these teeth in fetal nutrition. The teeth of oviparous embryos and larvae are similar to those of the adult, without marked ontogenetic variation (Sarasin and Sarasin, 1887-90; Marcus, ’20; Reuther, ’31; Lawson, ’65a,b; Wake, ’76), and there is considerable interspecific variation in adult dentition as well (Wake and Wurst, ’79), some correlated with feeding specializations (Wake, ’78). This system lends itself to 1) analysis of tooth

replacement phenomena, 2) comparison with tooth replacement analyses in other amphibians as well as in fish, reptiles, and mammals, and 3) consideration of current theories explaining tooth replacement and the evolution of tooth size, shape, and position in vertebrates.

This paper focuses on the ontogeny and replacement of teeth in Dermophis mexicanus, a Mexican and Central American terrestrial, burrowing, viviparous member of the gym- nophionan family Caeciliidae. All specimens are from a single population and were collect- ed a t various times of the year. Since gestation in this species is 1 year (Wake, ’80), virtually the entire pre-birth ontogeny as well as adult variation can be examined.

Parker and Dunn (‘64) described the fetal teeth of D. mexicanus as spoon-shaped with a single apical cusp. They commented that some populations of the species appeared to have multicusped teeth and reported that fetuses

0362-252518011662-0203$02.60 0 1980 ALAN R. LISS, INC.

204 MARVALEE H. WAKE

near birth size had dentitions of mixed fetal and adult teeth. Wake (‘76) described the teeth of a 22-mm D. mexicanus embryo and commented that the tooth crowns with long, flexible denticles and no mineralized pedicel may not be functional. It appeared that D. mexicanus, and other species, had two fetal tooth morphs. Current material available for study indicates that, through ontogeny, there is a transition from a multi-denticled “pref‘unc- tional” tooth crown through a reduction of cusps and an increase in enamel deposition and mineralization to the spoon-shaped, mono- denticled “functional fetal” form and then to the adult size, shape, and position on the jaws. The tooth ontogeny in this species is typical of live-bearing caecilians in many ways, but unusual in others, particularly in the ontogenetic changes in dentition as the fetus grows, as described below. The completeness of the series and the properties of the morphology provide an unusual opportunity for analysis of tooth growth and replacement. Several problems are addressed, utilizing the Dermophis mexicanus data and comparison with data from other caecilians, salamanders, frogs, liz- ards, and mammals. The pattern of change in fetal tooth crown morphology, the pattern of fetal tooth addition and replacement, and changes in the basic structure of the tooth during development are described and evalu- ated. The pattern of the transition from fetal to adult dentitional shape, size, and position, clues to the mechanism of this shift associated with developmental phenomena, and whether these patterns are self-generated (morphogenetic clones) or externally controlled (morphogenetic fields), or more complexly produced, are considered.

MATERIALS AND METHODS

An ontogenetic series of Dermophis mexicanus including embryos, fetuses, juveniles, and adults was prepared for study of dentitional and other morphology. Table 1 lists the specimens and their manner of preparation.

Preparation for scanning electron microg- raphy involved the technique described by Wake and Wurst (’79). Material was embedded in paraffin according to standard techniques and sectioned so that frontal, sagittal, and transverse series stained with hematoxylin and eosin and Mallory’s azan were available. Heads were embedded in plastic according to Lombard (’701, sectioned sagittally a t 10 pm on a standard microtome, stained with hematoxylin and safranin, and mounted individ-

ually. Other specimens were cleared and stained with alizarin Red-S or double-stained with alizarin and alcian blue (Wassersug: ’76). Tooth replacement series are much more eas- ily analyzed in cleared and stained than in dried skeletal specimens. Locus maps were constructed as in Wake (’76). In maps of fetal teeth, a teeth are the non-pedicellate, multidenticulate “prefunctionaYteeth; b teeth are the pedicellate, spoon-shaped, monocusped functional fetal teeth; B teeth are the transitional fetal-adult morph. Loci were counted as in Wake (’76). Type b teeth include b and c (labial, sloughing) types described by Wake (’761, since the significant morphological dis- tinction in D. mexicanus is between a and b types.

OBSERVATIONS

Tooth crown ontogeny Wake (‘76) described the tooth crowns of a

22-mm embryo of D. mexicanus as having several long, flexible denticles, being weakly mineralized, and lacking pedicels. It is appar- ent from new material that this is an early stage in tooth crown ontogeny in the species, as can be seen from the following sequence.

The dentary tooth crowns are in four rows antero-medially, reducing in number posteriorly on the dentary ramus (Fig. 1A). They are small, approximately 8 pm high (crown base to tip of longest denticle), and protrude little above the oral mucosa (Figs. 8a, b). There are two series of teeth in the roof of the mouth: a double row of multi-denticled teeth occurs on the ossifying maxillae and premaxillae, and a single row in a vomeropalatine series. These teeth show no alizarin affinity, so may be unmineralized.

Crowns are broader; denticles are reduced in height and frequently fused as paired units (Fig. 8c,d). The cup- or spoon- shaped face of later teeth is foreshadowed by the curvature medially of the outer margins of the tooth crowns (Figs. 8c, d, e). Some flexibility of denticles and the crown body is indicated by the variation in curvature of both components (Fig. 8d). Pedicels are forming.

Further denticle reduction is evident (Fig. 8e); the body of the crown is broad- ening and thickening. The apical denticles curve medially, and the lingual face of the crown is concave. Only the tooth tips are mineralized. There are four rows of dentary

35-mm fetus.

39-mm.

46-mm.

FETAL AND ADULT CAECILIAN TEETH 205

TABLE I , Specimens of Dermophis mexicanus prepared for dentitional analvsis

Total length in mm Maturation s ta te Preparation Tooth type

4 5 6

10 10 10 14 15 15 22 23 25 34 35 *35 38 *39 44

* 46 48 *51 58 58 *60 64 68 72 77 80 80

* 101 110 *110 * 120 * 123 140

* 141 * 148 * 150 * 151 155 162 164

* 185 199 265 290 325 327

* 349 398

a

Embryo Embryo Embryo Emhryo Embryo Embryo Embryo Embryo Embryo Embryo Embryo Embryo Embryo Fetus Fetus Fetus Fetus Fetus Fetus Fetus Fetus Fetus Fetus Fetus Fetus Fetus Fetus Fetus Fetus Fetus Fetus Fetus Fetus Fetus Fetus Juvenile Juvenile Newborn Juvenile

(2) Juvenile Fetus Juvenile Juvenile Juvenile head Juvenile head Juvenile head Adult head Adult head Adult head Adult head Adult head Adult head

Pa S Pa S Pa S Pa S Pa S Pa F Pa X Pa S Pa S Pa F C & S Pa X Pa F Pa X Pa F SEM C C S SEM Pa F SEM C & S SEM Pa X Pa F SEM D C & S Pa X Pa F SEM ~~

Pa X Pa F D C & S PI s D C & S D C & S D C & S D C & S D C & S D C & S D C & S D C & S D C & S P I F & S Pa F D C C S Pa F Pa F Pa F P l F & S Pa F C & S P1 s

PFF PFF PFF PFF PFF PFF PFF PFF PFF PFF PFF PFF PFF PFF P F F PFF PFF PFF PFF PFF FF

mixed PFF & FF mixed PFF & FF

FF FF F F FF FF FF FF FF FF FF FF + A FF + A A A A A A FF A A A A A A A A A A A

Abbreviations: A = adult; C & S = cleared and alizarin-stained D C & S = cleared and alizarin- and alcian blue-stained, F = frontal sections; FF = functional fetal; Pa = paraffin; PFF = prefunctional fetal; P1 = plastic; s = sagittal sections; SEM = scanning electron microscopy; x = transverse sections. Asterisks indicate specimens described in detail in the text; other specimens were prepared to provide more histological detail or other developmental stages for comparison.


the jaw. The overall dimensions of the crowns 4 F l 3 0) b' b2a2 are little changed from the 35-mm stage, but 2 b2 b' b' b' the shape is markedly changed. Teeth are in

five rows anteriorly on the lower jaw (Figs. l C , 8e). All of the teeth are well mineralized. Similar but smaller fetal teeth are disposed in four rows in a maxillary-premaxillary series and in four rows in a vomeropalatine series

A

I b' b' b' b' b'

B

- 4

C (Figs. 2A, 3A). b' b' b' 101-mm. Tooth crowns are predominately

the monocuspid, spoon-shaped type through-

labial 3 b b b b b b ! b b b b ; b b b b b b b b b 2 - B , b b b b b b b b b t

out the jaw. Multi-denticled crowns are present antero-medially and labially, extending posteriorly along the labial margin, but de-

b' b' b' b' b' b' V b' creasing in number posteriorly on the dentary.

110-mm. Dentary tooth crowns are predominately monocuspid and are in eight rows medially (Fig. ZD). However, seven teeth on the lingual anteromedial margin are larger, have a reduced apical cusp and a much shal- lower lingual face. These transitional teeth are designated type B. Each appears to occupy

5 I0 15 20 25 the equivalent of two of the spaces held by

b' b' b'

B b' B B b' b' b'

b b b b b

Loci posterior 4 smaller teeth. These teeth are momholoeicallv

I - , ,b, , , ,B,B: ,B, , , ,B, , , ,b, , ,b, , ,b

Fig. 1. Locus maps of fetal teeth on the right dentary ramus of Derrnophis rnezicanus. A) 35-mm specimen; B) 46-mm specimen; C) 64-mm specimen; D) 110-mm specimen; E) 151-mm specimen. Abbreviations: a, b, and B as described in the text. A numerical superscript indicates the cusp number (superscript indicates a multi-cusped tooth), absence of superscript indicates that all are monocusped, and e indicates that the crown is just erupting.

teeth (Fig. lB), the labialmost having developed earliest; three rows of maxillary-premaxillary teeth and a single row of vomeropalatine teeth.

51-mm. Many tooth crowns are highly curved, relatively stout-bodied, and have a single medial apical cusp. These are well mineralized, as shown by alizarin staining, and have mineralized pedicels. An anterior labial view (Fig. 8f) shows several such teeth and one, closest to the labial margin, that lacks the medial apical cusp but has virtually no lateral denticles. On the posterior lingual aspect of the same jaw (Fig. 8g), the largest, thickest, most concave crowns are those with the single apical cusp; those more posterior and more labial are similar to crowns of the 35- to 46-mm specimens. This is of significance to the tooth succession proposed below. The crowns form five to six rows on the lower jaw.

Crowns of the concave, monocusped type predominate along the length of

64-mm.

lingual

more like adult than fetal teeth 6ut lGk th; lateral flanges and slight convexity shown by Wake and Wurst ('79). In the maxillary-premaxillary series there are four rows of fetal teeth, with five adult-like teeth interspersed medio-laterally in the first and second rows a t loci 2, 7, 8, 10, and 14 (Fig. 2B). The vomeropalatine series is of fetal teeth in four rows, with a single adult-type tooth at locus 10 in the first row (see Fig. 3B).

The fetus has a full complement of cusped fetal teeth. They are disposed in six rows from lingual to labial aspect antero-me-

120-mm.

6 b b b b b b b b b b 5 B b b b b b B b b b b b b : - B B b B b B b b b - B Be B B. b

2 b b b b I , , , , b , , , , , , , , , , B: , , , , , , , , , b', , b',

I 5 10 15 20 25 LOCI posterior -

Fig. 2. Locus maps of fetal teeth of the left maxillary- premaxillary row. A) 64-mm specimen: B) 110-mm specimen; C) 151-mm specimen. Abbreviations as in text and Figure 1.

FETAL AND ADUL'I' CAECILlAN

A

2 b I be

~ ~ , b , , ~ , ~ ~ , b , b , : , B 8 ,b!; j!, ,!, ,:,:,I,:, , 1 2 b B b b' B b b b b b I b b b ' b b b b b '

I 5 10 15 20 25 Loci posterior -

Fig. 3. Locus maps of fetal teeth of the left vomeropalatine row. A) 64-mm specimen; B) 110-mm specimen; C) 151-mm specimen. Abbreviations as in text and Figure 1.

dially, reducing to three, then one, posteriorly on the lower jaw and in the maxillary-premaxillary series.

This free-living juvenile has a full complement of adult teeth arranged in single rows (Fig. 4A, B, C).

This 2-day-old specimen has a full complement of adult teeth as above, but is also sloughing medially and labially its remaining fetal teeth.

This juvenile has a full complement of adult teeth.

A juvenile has a full complement of adult teeth (Fig. 5A, B, C).

This large fetus has a full set of fetal monocusped teeth in up to eight rows medially on the lower jaw, six and five in the maxillary and vomeropalatine series, respec- tively. It resembles the complement in the 110-mm fetus, but includes greater numbers of large functional fetal teeth and of the transitional tooth type (Figs. lE, 2C, 3C).

This advanced juvenile has nor- mal adult teeth (Fig. 6A, B, C).

The complement of adult teeth is present, numerically greater in both functional teeth and replacement stages than in smaller specimens (see Fig. 7).

Other aspects of tooth crown morphology are considered based on analysis of 1) anomalous development, and 2) crown structure as revealed by accidental SEM beam damage as a result of overexposure. One tooth in the 35- mm fetus (Fig. 8a, left middle of field) showed

123-mm.

141-mm.

148-mm.

150-mm.

151-mm.

185-mm.

349-mm.

e - d

b m C

a

Loci posterior 4

Fig. 4. Locus map of teeth in various successional stages in a 123-mm juvenile D. mexicanus. A) Right dentary ramus; B) left premaxillary-maxillary row; C) left vomeropalatine row. Stages a-d, erupting to assuming fixed position; e is an ankylosed functional tooth; f is a tooth in which the pedicel is eroding; g is the space left by a sloughed tooth. See Wake ('76) for more detail.

an irregular surface and single medial extension (Fig. 9b). Similar tooth crowns were ob- served, although infrequently in other specimens. This tooth lacks an enamel layer and therefore lacks the denticles typical of teeth in this size fetus. The irregular crown surface is assumed to be due to irregular pulses of dentine deposition as the tooth forms. The crown from a 77-mm specimen that suffered beam damage is shown to have an internal dentine structure similar to the tooth from the 35-mm specimen mentioned above. The tooth appears to have enamel that is lain down in three coats with slightly different orientation in this specimen. Based on examination of internal and external lamellar cells of tooth buds of small specimens, there appears to be a correlation between number of dentine pulses (surface blips) and lamellar cell counts. This suggests that the dentine "core" of all fetal teeth is similar, and crown cusp variation is a property of change in enamel deposition with increased age in this species. Microana- tomy of tooth development is the subject of another manuscript.


A 0

:Cl f

Fig. 5. Locus map of teeth in various stages in various successional stages in a 150-mm juvenile. A) Right dentary ramus; B) left premaxillary-maxillary row; C) left vomeropalatine row. Stages as in Figure 4.

Fetal and adult tooth replacement Tooth replacement patterns in D. mexicanus

are similar in many ways to patterns described by Wake ('76) for Gymnopis, Typhlo- nectes, and Schistometopum. 'Ibvo sets of fetal teeth are present; numbers of teeth may increase as new loci are added anteriorly before the jaw is mineralized early in development and posteriorly afterward; numbers of rows of teeth increase as age increases, although pedicels do not fuse to form the dentary patch seen in Typhlonectes. Observations will therefore be confined to those aspects in which D. mexicanus either differs in pattern or adds new information about replacement patterns.

A major difference in tooth crown morphology exists between type a prefunctional teeth and type b functional teeth in D. mexicanus. The former are multi-denticulate and fairly flat-faced, with pedicels that are unmineralized to weakly mineralized. The latter, monocusped and concave lingually, with stout, well- mineralized pedicels. The "functional" desig- nation refers to tooth use in oviducal feeding (Wake, '76). This is unlike other species reported by Wake, in which the prefunctional tooth crowns are miniatures of the functional crowns.

b e 0 , , , , 0 , , , , , , , ,

C g . 0 :.' ,*;,*,*,:;;;; ;, , , , ,

b 0

5 10 15 Loci posterior -

Fig. 6. Locus map of teeth in various stages in a 185- mm juvenile. A) Right dentary ramus; B) left premaxillary- maxillary row; C) left vomeropalatine row. Stages as in Figure 4.

D . mexicanus is unusual in having both maxillary-premaxillary and vomeropalatine tooth series present during the fetal period. In other species the maxillary-premaxillary series occurs late in fetal development, if at all, and the vomeropalatine series is not represented. As noted above, the latter two series of teeth increase in numbers of teeth and numbers of tooth rows in a pattern similar to that of the lower jaws (compare Figs. 2 and 3). Prefunctional a teeth occur in the labialmost tooth rows in all three series, presumably the result of aggregation of progressive teeth in loci from the more lingually situated dental buds. Several functional fetal teeth aggregate in each tooth family and are slowly sloughed. This contrasts with the adult state of a single functional tooth per family. Multiple functional teeth are typical of all fetal dentitions examined.

The several fetuses near birth size, new- borns, and juveniles yield considerable new information about the fetal-to-adult dentition- a1 transition. Birth occurs between 108 and 155 mm fetal total length, usually between 125 and 140 mm (Wake, '80). The teeth of a 110-mm fetus, a 123-mm juvenile, a 151-mm fetus, and a 150-mm juvenile are mapped for


Loci posterior +

Fig. 7. Locus map of teeth in various stages in a 349- mm adult. Right dentary ramus. Stages as in Figure 4.

comparison (Figs. 1-51, and other specimens, fetal and free-living, in this range were prepared and examined (see Table 1). A key feature of both the 110-mm and the 151-mm fetal dentitions is the presence of teeth that resemble the adult morph (type B ) more than the type b morph. These are interspersed among b teeth in all three tooth series. The larger fetus has more numerous teeth of both types in more rows (except for the dentary) than the smaller (Figs. 1-3). The transitional teeth are much larger (two times, in both height and breadth of crown) and at nearly equally spaced intervals on the jaw. In most tooth series of both specimens, more anterior (medial) B teeth are in more lingual tooth rows. This suggests that the transition begins anteriorly on the jaw and subsequently develops posteriorly. However, in the vomeropalatine row, it appears that the first B tooth is not most anterior. The only B tooth in that row in the 110-mm specimen is in the tenth locus (first on the palatine element); a B tooth in locus 10 (last on the vomer) of the 151-mm specimen is in a near-labial row, whereas the other two B teeth, one more anterior and one more posterior, are in lingual positions.

A comparison of the 123-mm, 150-mm, and 185 -mm juveniles (Figs. 4-6) shows that number of functional adult teeth of the lower jaw is about the same in each (9, 12, and 11 on the right ramus), whereas the number increases with increased size in the other two tooth series. This suggests that there is a fundamental tooth complement for adult feeding, and that there is high significance to the dentary complement. The proportion of earlier developmental stages of teeth also increases with age, as noted by Wake ('76) for other species. The large (349-mm TL) mature specimen (Fig. 7) has only one more functional dentary tooth, but two to four more loci are involved and many more replacement stages are present; maxillary and vomeropalatine series show greater numbers of functional and replacement teeth as well.

DISCUSSION

Developmental shape-transition sequence The earliest tooth crowns are tiny structures

with a dentine base and a thin enamel layer extended somewhat irregularly into a number (three to seven) of apical spikes. These crowns are not mineralized or are weakly mineralized and are not ankylosed. They are shed during the later fetal period. This state is similar to the situation that Osborn ('71) noted in pre- hatching embryos of Lacerta. The developmental sequence involves restriction of the number of enamel apical spikes so that two occur in early functional fetal teeth. These sequential changes are described below and can be followed in the developmental series shown in Figure 8. The breadth of the body of the tooth crown increases. There is also an increase in curvature of the two sides of a crown toward each other so that a concave lingual aspect is achieved. This also brings the spike regions into closer proximity (Fig. 8d). The increase in crown breadth and thick- ness and reduction of denticle or spike height results in the crown configuration shown in the tooth in the upper righthand corner of Figure 8e. Crowns produced subsequently have the lateral apical regions fused lingually to produce the enclosed spoon shape and a new, single apical extension. This is suggested by comparison of labial and lingual aspects of teeth in Figure 8f-h. Since it appears that the dentine base component of the crown is only slightly curved and has either a single median or paired extension in close proximity (Fig. 9a, b), much of this variation may be due to the developing nature of enamel deposition. Size of crown and breadth of dentine and enamel layers increase as cell number (to a limited degree; see Meredith-Smith and Miles, '71) and output increase. The transitional fetal-adult tooth is larger in size, more flattened, and without the pronounced apical spike of functional fetal teeth. It may be construed to be the result of further maturation of the dental progenitor, suppressing the spike and strengthening the body of the crown so that its sides do not curve medially, resulting in a flatter, more conical tooth. These transitional teeth are smaller than posterior (new) adult teeth and lack the lateral flanges typical of the arrowhead-shaped tooth crowns of the species (Wake and Wurst, '79).

Properties of the tooth recruitment sequence are also evident in Figure 8. In Figures 8c, e, f, and g, it can be seen that the multi-cusped,

210 W V A L E E H. WAKE

Figure 8

211

Fig. 9. Scanning electron micrographs of anomalous fetal tooth conditions. a) Crown in a 77-mm specimen in which beam damage has caused the enamel layers to shear away from the dentine. Note the single apical spike and the irregular surface of the dentine. b) Crown in a 35-mm specimen (also shown in Fig. 8a) in which enamel was not deposited over dentine. Note the curvature of the crown and the medial and apical dentine elongations. Bar = 10 pm. See text for discussion.

Fig. 8. Scanning electron micrographs of fetal teeth of the right dentary a t various sizes and stages of development. a) 35-mm specimen, anterior lingual view; b) 35-mm, posterior lingual view; c) 39-mm, posterior lingual view; d) 39-mm, mid-ramus lingual view; e) 46-mm, anterior labial view; f) 51-mm, anterior labial view; g) 51-mm, posterior lingual view; h) 60-mm, posterior lingual view. Bar = 10 pm in all micrographs. Compare the cusp numbers and curvature of the crown faces as size of fetus increases. Note in c and g that multi-cusped crowns, which erupt earlier, are on the labial margin of the jaw relative to later-erupting, larger crowns that have fewer cusps and are in more lingual series. Arrow in 8a indicates tooth enlarged in Figure 9b.

212 MRVALEE H. WAKE

flatter-crowned tooth characteristic of early stages of development is labial to the later, functional, mono-cusped, spoon-shaped morph. The multi-cusped tooth therefore is assumed to be crowded labially as successive rows of more mature fetal teeth accrue. Yet, the pos- teriormost new loci, added in more advanced fetuses, do not replicate the entire sequence of tooth development. Frequently the first tooth of such a new locus is a type b tooth (as in Fig. 8h), suggesting that there is a matura- tional phenomenon affecting the entire dental primordium, organized or not.

The transitions from a to b tooth crown types, and to B and adult, are cued to other transitions in the development of the orga- nism. The a to b transition (prefunctional fetal tooth to functional) occurs as yolk is exhausted by the embryo (at approximately 25 mm total length). The fetus shifts to in- gesting the nutrient secretion of the oviducal epithelium, and the fetal teeth are indeed functional (Wake, '77a,b). Type B teeth accrue in fetuses 110-160 mm, but just before birth. The size and placement, including spacing, of these teeth foreshadow the state of the adult tooth. Birth in this species is correlated with the onset of the rainy season. Fat bodies of large fetuses are very small, so it is inferred that feeding upon invertebrate prey should be established shortly after birth (Wake, '77a,b, '80).

The presence of the vomeropalatine series in fetuses of this species suggests that this is a function of dental primordium organization, not of functional involvement. If Wake ('76, '77a,b) and Salthe and Mecham ('74) are cor- rect, the protruding teeth of the maxillary series and especially the dentary are used to stimulate secretion from oviducal epithelial cells. The vomeropalatine teeth do not partic- ipate in this function. That the marginal rows of teeth are so involved is corroborated by the presence of shredded epithelium and especially of red blood cells, presumed of maternal origin, as seen in Figure 8f.

As noted above, a number of aspects of tooth development and replacement are typical of other caecilian species and of lower vertebrates with polyphyodonty and indeterminate growth in general. Tooth loci are added anteriorly until the jaws mineralize, and posteriorly on the jaws subsequently. In fetuses, tooth rows aggregate on the jaws, showing maturation sequences, and sloughing is slow. New tooth types or earliest maturation occur anteriorly (medially). However, the inception

of the B tooth in the middle of the vomeropalatine row may be similar to the mid-jaw stem progenitor position Osborn ('71) found in Lac- erta. Further, D. mexicanus is not typical of viviparous caecilian species in having a ma- turational sequence of fetal and adult tooth types. As noted above and in Wake ('761, in most other species, the nonfunctional fetal tooth crowns are smaller but of the same shape as the functional fetal teeth. In addition, there are several reports (see Parker and Dunn, '64) of the presence of fetal teeth in free-living specimens, without indications of teeth of transitional form to the adult. It is therefore possible that fetal tooth morphology is often more genetically "fixed" than in D. mexicanus, and that the transition from fetal to adult shape and position is a more abrupt and radical change. However, prebirth ontogenetic series are not yet available for other species, and the virtually complete D. mexicanus series provides substantial insight into fetal tooth development, although there may be some variation in timing and pattern among viviparous caecilian species. Several problems of interpretation of tooth maturation and replacement arise: First, that of explaining the different patterns of replacement of fetal and of adult teeth; second, explaining the difference in pattern of organization (position) of adult vs. fetal teeth; third, explaining the shape transitions and changes in function, correlated with other developmental properties. If adult teeth (since they are a single tooth class as defined by Osborn "781) have a single primordium, as suggested above, does this mean that the primordium is different from that of the fetal teeth with which it is surrounded, or is it a maturation phase of a pre-existing primordium? The above questions, and the data presented herein, will be interpreted according to current theories of tooth development and replacement, primarily the morphogenetic field theory (including Ed- mund's "601 Zahnriehe theory) and the morphogenetic clone theory, both as defined by Osborn ('78).

The field theory and the clone theory Both theories have been proposed to account

for ontogenetic differentiation of regions, units, shapes, sizes, and sequences of teeth. Major distinctive properties of the two ideas, as summarized by Osborn ('78), are as follows: 1) patterns controlled from extrinsic sources (field) vs. self-generated (clone); 2) all primor-


dia equivalent, but influenced by field substances (field) vs. all primordia different, with final shape largely predetermined (clone); 3) primary gradient (field substances) inducing development of a secondary gradient (shape) vs. gradients being concomitants of growth.

With regard to tooth development, the field theory would have a specialized field generator anteriorly on the jaw, or presumptive jaw, which produces a field substance that diffuses through the growing region or dental lamina. The further a cell is from the field generator, the less field substance it is exposed to. Tooth primordia differentiate, probably due to a different field effect, and the identical primordia are subject to different concentrations of field substances due to differences in distance from the field generator, so that a gradient of structure is produced.

In the clone model, tissue equivalent to the field generator contains three regions, the middle one of which gives rise to primordia and the tissue surrounding them. The middle region is the clone, and it grows posteriorly. Cell division ensues, and the tissues become competent t o initiate primordia (suggesting a maturation effect). The clone expands posteriorly, and new primordia arise as space be- comes available within the cell region called the clone. Osborn ('71, '74b, '78) suggests that a zone of inhibition develops around a primordium, restricting development of new primordia nearby. Later primordia (interspersed anteriorly in growth space and added posteriorly) are derived from cells that have divided more times than those of earlier, more anterior primordia, so that gradients in regional structures (such as anterior vs. posterior teeth) are the result of a gradient in cell ancestry.

Tooth shape, according to the field theory as discussed by Butler ('39, '56) and Van Valen ('701, is thought by those authors to be the result of the ectodermal enamel organ and the mesodermal dental papilla folding into a shape that approximates the shape of the later tooth. Sites that will develop into tooth cusps mature earlier than surrounding tissue, and so have different sensitivities to field substances. The clone theory does not require sensitive, or target, sites. Osborn ('74b) proposed that the enamel epithelium grows over the surface of the dental papilla a t a constant rate in all directions. The dental papilla grows at constant, but different, rates in various directions, so that the shape into which the enamel organ folds is dependent on the growth of the dental papilla. The clone theory, then,

says that the shape of a tooth is determined by the growth rate of the primordium and, ultimately, the clone. Shapes therefore may be different but graded. "Shape potential" of cells in a clone therefore changes as the clone matures and extends. Some clone cells do not become incorporated into primordia. Osborn ('78) presents experimental evidence to show that all cells of the dental papilla have the same developmental information, so that shape is intrinsic.

Considerations of tooth number by Osborn ('72, '74a,b, '77) are aimed at interpretation of the evolution of diphyodont, heterodont mammalian dentitions from polyphyodont, homo- dont reptilian precursors, but contrasts between field and clone theories can be made. According to field theory, response to field substances peaks at various places along the jaw, resulting in a number of teeth, or, as Osborn ('78) interprets Wolpert ('69), a gradient of field substance gives "positional information" and cells respond to specific concentrations of field substance, thereby giving rise to evenly spaced teeth. The clone theory pro- poses that primordia can be initiated anywhere in the clone, but once initiated, gener- ate a zone of inhibition, giving a spacing of developing teeth. Few primordia can develop in small clones or those with large inhibitory zones, so the number is self-generated.

Sequence of tooth initiation is controlled by an external substance, such as diminished field substance producing later or smaller teeth (field theory). The clone theory holds that new primordia arise at the margins of the extending clone, and shape potential of new primordia is the result of cell ancestry.

Tooth loss during evolution is attributed to weakening of the field effect (field theory) or a reduction of shape potential of clone cells below a threshold before the clone finishes growing, so that primordia are generated but do not develop (clone theory). According to the latter, teeth are lost in sequence from the margins of tooth classes (for example, incisors and canines) generated by the clones.

There are many similarities between the D. mexicanus data and those for Lacerta uiuipara, the viviparous lizard carefully analyzed by Osborn ('71) which provided the basis for much of the presentation of the clone model. Many of the developmental phenomena shown in D mexicanus can be interpreted according to the clone model, but, a t the same time, the data invoke questions not answerable by clone theory, but by a field model.


The sequence of initiation of fetal teeth is anterior to posterior, appropriate to either theory. Posteriorly on the jaw, primordia gen- erate type b teeth without going through an a stage. This is particularly logical according to clone theory, for these primordia are generated at the margin of the growth unit and may be the result of greater numbers of cell division, thus an alteration of the cell ancestry, so that the more advanced tooth type is developed. Yet, a major question arises from this idea. I t is assumed that cells giving rise to later primordia have divided more frequently than those of earlier primordia (Osborn, ‘78, p. 173). Why is this necessarily so? The jaw itself organizes anteriorly in caecilians, with extensive differentiation and cell division (Marcus, ’20 Wake, unpublished), so that posteriorly, there have been fewer cell divisions at the same point in time. Posterior dental buds form before the jaw is well-organized. It is a t best possible that these are the results of as many divisions as more anterior buds, but more likely fewer, as they appear later. This is not just a growth phenomenon, but one of differentiation as well. Osborn (’78, p. 175) also suggests that the clone may grow pro- gressively more slowly, so that the growth rates of the tooth primordia are equivalently reduced in initial growth rates, resulting in graded shapes of teeth. This suggests that there would result smaller or more embryonic teeth, not the more advanced type found in caecilians.

The phenomena of multiple rows of fetal teeth in caecilians (see Wake, ’76) and tooth patches in other forms (for example, in the plethodontid salamander Eurycea described by Lawson et al., ’711, and the transition to the adult single rows of teeth, is poorly reconcilable to the clone model. For fetal teeth to aggregate in the manner that they do, there must be very weak “zones of inhibition” generated to provide spacing. In fact, spacing, especially in terms of numbers of rows (teeth produced per locus), seems unregulated, and is mediated only by birth. Spacing of B teeth seems to take up the equivalent of three to four loci of fetal teeth; hence, a “zone of inhibition” might be postulated. However, the sudden increase in this phenomenon a t birth is not explained by the clone theory. The reduction in numbers of teeth per row and in numbers of rows also cannot be reconciled to this theory. The clone model predicts that teeth are lost sequentially a t the margins of tooth classes generated by clones. It appears

that teeth of the lower jaw of D. mexicanus represent a single class, and therefore a single clone, by analogy to Osborn’s L. viuipara, so tooth loss should be posterior, not interspersed throughout the jaw. The “zone of inhibition” weakens as a tooth ages, so that alternate replacement may occur. It is not known to totally suppress loci so that the teeth are lost.

Tooth shape itself is poorly explained by the clone theory. The earliest fetal teeth in D. mexicanus are nonfunctional, as are those of L. vivipara (Osborn, ’71). Osborn suggests that shape potential in Lacerta decreases early in life to a minimal level represented by simple conical teeth, accounting for the loss of tiny accessory cusps on the teeth of hatchlings. Such an explanation might be invoked for the overall shape transition in Dermophis, but does not explain the differences in tooth shape correlated with feeding function in fetus vs. adult. Osborn (’78, p. 81) comments that while the idea that sequences evolved in response to the requirements of the animal suggests se- lective advantage for the sequence, it does not indicate the control mechanism. Yet, Osborn’s control mechanism, I infer, would involve reg- ulation of change on the margins of clones. This may apply to a series of heterodont teeth in a mammal, with each type derived from a different clone, but is weakly applicable to the caecilian ontogenetic sequence. A shape transition has been hypothesized for these teeth, suggesting that they represent a single clone and a single tooth class, but change in tooth types does not occur at the margins of clones. This does not explain the timing of the fetal- to-adult change, or the change from the nonfunctional fetal to the functional form, both of which are correlated with major changes in nutrition. Surely, “shape potentials” may change as cell “competency” increases. How- ever, this does not control or mediate change, but is another product of change.

Osborn (‘78, p. 185) indicates that tooth shape potential and size are affected by hormones, citing evidence from the literature on salamander sexual dimorphism and seasonal change (although he inappropriately suggests that such effects might not be a valid conclu- sion from the data). He does not explain the nature of hormonal influence. It is surely an “external” difference, so it calls into question the degree to which shape is intrinsic. The situation in caecilians is clearly one in which hormones play a part. The change from yolk nutrition to that of the maternal oviducal secretion is at least indirectly hormonally me-

215 FETAL AND ADULT CAECILIAN TEETH

diated. The female’s corpora lutea produce considerable progesterone during the time that oviducal secretory activity is maintained (McCreery, personal communication). Secre- tory activity probably diminishes shortly before birth (Wake, unpublished), so fetuses may be subject to a reduced progesterone level as well. A metamorphosis occurs in the oviduct in fetal caecilians, involving loss of gills (Wake, ’67), changes in the structure of the eye and the skin, inception of the tentacle, and change in hemoglobin (Toews and Macin- tyre, ’77). I have no reason to doubt that this is under the control of thyroxin and prolactin, as is typical of all amphibians investigated thus far. The transition from fetal to adult dentition, which begins in the oviduct shortly before birth, is likely under similar hormonal control. This aspect is similar to the field model, in which tooth shape, etc., are induced. An anteriorly placed “field generator” of un- known origin need not be postulated, since maturation of teeth is consistently anterior in most tooth series, so that more mature loci probably respond earliest to hormonal presence. In fact, the most mature locus anywhere on the jaw would probably respond first. An- other aspect of tooth initiation reconcilable to the field model has to do with the nature of differentiation and organization on the jaws and dental laminae. Since differentiation is anterior first, proceeding posteriorly, it is likely that either “inducer” substances or the byproducts of newly differentiating cells are the equivalent of Van Valen’s (’70) several different field substances, since they would have a directionality along the jaw as a result of developmental timing.

Finally, many of the arguments are based on interpretations of the genome and its re- sponses, without any substantive knowledge of the nature of the genome. Some recent experimental embryology sheds some light on this problem (for example, Kollar, ’78; Miller, ’78; Flynn-Miller and Miller, ’78; and the work of their collaborators), but not to the point that it deals with the questions raised by Osborn and herein.

Aspects of both the clone model and the field model are useful in interpreting the Der- mophis data. Osborn (’78) believes that the field model is often applied to any aspect of variation and does “little more than disguise the statement of an observation as an explanation,” and lacks predictive power “because fields seem to be infinitely variable.” I suggest that the clone model, while explaining certain

developmental phenomena of dentitions, has serious weaknesses as well. I suspect that a biological explanation of these phenomena will involve reconciliation of some aspects of both extant theories in a model that also includes information on the genome and hormonal and other extrinsic mediation.

ACKNOWLEDGMENTS

I thank Gloria Wurst for taking the scanning electronmicrographs and sectioning many heads, Willy Bemis for preparing heads according to several techniques, and other as- sistance. I appreciate the use of facilities, equipment, and advice of the Electron Micro- scope Laboratory at the University of Califor- nia, Berkeley. I am grateful to John Cadle, Theodore Papenfuss, Robert Seib, David Wake, and Thomas Wake for collection of specimens, and to David Wake for criticizing the manuscript. All material will be deposited in the Museum of Vertebrate Zoology, Uni- versity of California, Berkeley. I also thank Diane Nakamura for typing the manuscript and Gene Christman for preparing the graphs.

This work was supported by National Sci- ence Foundation grant DEB 77-22642.

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