Biological Journal of the Linnean Society, 9: 217-229.With 7 figures
September 1977
The interpretation of patterns in dentitions
J. W. OSBORN
Unit of Anatomy in relation to Dentistry, Anatomy Department,
Guy’s Hospital Medical School, London SEI 9RT
Accepted for publication May I977
Studies of the fossil record indicate the sequence in which the shape of a phenotype has
been modified during phylogeny. These data can provide a valuable starting point for
theoretical embryology. Any theory which accounts for the development of a particular
shape or pattern in recent animals should, by equivalent modifications, be able to account
for the phylogenetic sequence of shapes. This argument is illustrated by the evolution and
development of patterns in dentitions.
KEY WORDS: - teeth
inhibition - alternation.
- dentitions
- patterns - evolution
- ontogeny - Zahnreihe -
CONTENTS
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Taxonomy and embryology
Patterns of tooth replacement
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The control of alternation . . .
The relationship between patterns
Captorhinomorphs
. . .
Testing the model
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References
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TAXONOMY AND EMBRYOLOGY
It is generally true that during progressive evolution the physiology and
anatomy of vertebrates becomes increasingly complex. Each modification
overlies and to some extent obscures an ancestral simplicity which will
never be regained. In the same way it is probably safe to assume that the
ontogeny of nearly all recent vertebrates is more complex than the
ontogeny of their ancestors: daughter taxa are the successful variants of a
mother taxon and it is generally to be expected that the variants would be
more complex. So the simpler ancestral mechanisms of development are
progressively obscured beneath generations of modifications. Partly for this
reason remarkably little is understood about the fundamental mechanisms
of development and their control.
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217
J. W. OSBORN
218
Clearly it is not possible to study development in a fossil species, but
the changes in the shape of a particular structure developed in a phylogenetic sequence of animals could provide valuable data concerning the
controls which may have operated during its development. The following
analogy may help to explain this.
A shape which is very like a rectangular hyperbola can be produced by
rounding the point of contact between two lines which meet almost at a
right-angle (Fig. lA,B). The apparently close relationship between these
shapes gives no hint of the entirely different mechanisms required to
develop a right angle and a true rectangular hyperbola. To understand the
‘embryology’ of the hyperbola it is first necessary for a ‘palaeontologist’ to
have discovered and described circles, ellipses and parabolas (Fig. lC,D).
Figure 1. A. Two lines meeting at right angle; B, rectangular hyperbola; C, parabola; D, ellipse;
F, catenary. The shapes 8,C, D and a circle are closely related: each is produced by sectioning a
cone at different angles (E). Although A and B, and C and F, look very alike they are totally
unrelated shapes.
Next a ‘phylogenetic taxonomist’ concluded from &e tenets of his discipline that the circle ellipse, parabola, and hyperbola are sequentially
related. The ‘theoretical embryologist’ discovered that each shape can be
produced by sectioning a cone at increasing angles (Fig. 1E). The discovery
of this cone ‘control’ warns the ‘taxonomist’ not to include a catenary,
the shape assumed by a chain which is suspended by its two ends
(Fig. lF), nor a right-angle, in the same ‘taxon’ as the four conic sections
because they are generated by entirely different developmental controls.
The rectangular hyperbola and the right-angle, and the catenary and
parabola are each examples of ‘convergence’: they are closely related by
shape but not by ‘embryological’ or ‘evolutionary’ origin.
From the above argument I suggest that the first step towards understanding the relationship between dentitions is to describe their organization. A phenetic taxonomy which arranges and classifies groups according
to likeness can be constructed from these descriptions but may or may
not indicate the most accurate relationship. The next step is to suggest a
minimum number of controls, slight variations in which could account for
the greatest number of different shapes. If these controls have been
correctly discovered, the true relationship between different shapes will be
known.
PATTERNS IN DENTITIONS
219
PATTERNS O F TOOTH REPLACEMENT
The teeth of most non-mammalian vertebrates continue being replaced
throughout life with the result that the jaws always contain developing,
erupting, and functioning teeth. Each new tooth is initiated deep inside
the jaw and as it grows it passes towards the oral cavity where it
functions for a few months before being replaced from below. The
developing and erupting teeth are usually arranged with a geometrical
precision which is at first sight difficult to appreciate (Fig. 2A): the
arrangement is easier to visualize if the functioning teeth are ignored
(Fig. 2B). The pattern is precise and results in a condition known as the
wave replacement of alternate teeth. This refers to the fact that the teeth
are replaced in waves which sweep through alternate tooth positions from
the back to the front of the jaw (e.g. positions 11, 9, 7, 5, 3, and 1 in
Fig. 2A), although the waves pass from front to back in some species. The
wave replacement of alternate teeth, which I will refer to simply as
alternation has been most extensively documented by Edmund (1960) but
many others had previously observed it; e.g. Bolk (1912), Woederman
(1919), Parrington (1936), Romer & Price (1940).
A selective advantage for alternation may be that it allows the
maximum number of teeth to be fitted into the space available in the
jaws. A more irregular pattern of development and replacement could
result in the presence of unacceptably large, albeit temporary, spaces along
the tooth row (Romer & Price, 1940; Osborn, 1971).
In most animals the plane of the alternating pattern is vertical (Fig. 2E)
so that only the teeth at its edge are functioning. In many of the
Batoidea (rays and skates) the alternating pattern is spread over the surface
of the jaw (Fig. 2D). New teeth are developed deep on the lingual side of
the cartilaginous jaws and added to the posterior edge of a carpet of teeth
which rolls into the mouth. At the anterior margin of the jaws teeth are
removed from the carpet and shed to the ocean floor.
The only other common replacement pattern is that adopted by most
mammals. Because mammals have only two sets of teeth, deciduous and
permanent, it is only possible to observe sequences of development in
embryos and sequences of eruption in young animals. In most eutherian
mammals the incisors develop and erupt in sequence from front to back,
the deciduous molars in sequence from back to front and the permanent
molars in sequence from front to back (Osborn, 1971) (Fig. 4D). There is no
observable co-ordination between the eruption of the three incisors, the canine
and the seven molars. In polyprotodont metatherians the upper third incisor
(13) is the first to develop and is followed by 14, I5 and 12, I1 (Berkowitz,
1967).
A few animals erupt their teeth in sequence from the front to the back
of the jaws: for example, the agamid lizards (Cooper, Poole & Lawson,
1970) who do not replace their teeth and the piranha fish (Berkowitz,
1975) who do replace them. The gomphodont cynodont, Diademdon,
from the lower Triassic seems to have replaced each postcanine five times;
the teeth being replaced in sequence from front to back (Osborn, 1974a).
Recently Bolt & De Mar (1975) have described an unusual pattern of
J. W. OSBORN
220
0
I
2
3
4
5
6
7
8
9
10
II
12
C
Figure 2 A. Diagrammatic appearance of the functioning dentition above and the developing
replacement teeth below in a homodont polyphyodont animal. Anterior is to the left. The teeth
develop deep in the jaw and.pass to the surface as they enlarge. They are finally resorbed and
lost ahead of a newly erupting tooth. B. The developing teeth are arranged in a very regular
pattern. A Zahnnfhe, tooth family and replacement wave are indicated. The alternating pattern
can be generated by multiple Zahnreihen (or tooth families, or replacement waves). C. The same
pattern can also be produced if each developing tooth, black circle, is surrounded by a zone
which inhibits the initiation of a new tooth. The position of each tooth, for example the
square, is determined by the inhibitory zones surrounding the adjacent three earlier developed
teeth. The alternating pattern is self-generating. D. In rays and skates the alternating pattern is
spread over the surface of the jaw. E. In most animals the pattern is vertical so that only the
teeth at its edge are functioning.
PATTERNS IN DENTITIONS
221
tooth replacement in Cuptorhinus uguti from the lower Permian. This
dentition will be discussed later.
A mixture between the mammalian pattern and alternation is seen in
Thrinaxodon, a mammal-like reptile from the Triassic. A large canine
separates precanines in front from postcanines behind. Like reptiles, the
teeth were replaced throughout life but like mammals there was no
apparent co-ordination between the eruption patterns in the three different
regions. Wave replacement of alternate teeth persisted in the precanine and
postcanine regions (Fig. 4C). This dentition has been analysed by Osborn &
Crompton (1973).
The above list includes almost all the observations which have been
made of tooth eruption and replacement sequences. It is difficult to
understand how the somewhat irregular pattern seen in mammals is related
to the ancestral alternation. But the patterns have been described and it is
now possible to make the next step; to suggest a plausible control whose
modification could account for the development of the different patterns.
THE CONTROL OF ALTERNATION
Edmund (1960) used his observations on alternation t o construct a
theory of developmental control. He suggested that a stimulus is initiated
at the front of the jaw and slowly passes back through the jaw. Whenever
the stimulus encounters a tooth position it initiates the development of a
new tooth. The row of teeth developed in response to this stimulus
constitutes a Zuhnreihe. Throughout life new stimuli are regularly initiated
at the front of the jaw so that at any one time several Zuhnreihen are
being developed as successive stimuli sweep backwards (Fig. 2B). Surprisingly, if the timing is accurate this sequence of development leads to
alternation. Based on his theory of developmental controls, Edmund
suggested that a Zahnreihe is a structural unit of dentitions.
Osborn (1971) offered a different theory which he subsequently
developed further. He suggested that the presumptive tooth bearing regions
of an embryo consist largely of potential tooth forming cells which are
constantly proliferating. Whenever a tooth is initiated it is surrounded by a
region in which the initiation of a new tooth is temporarily inhibited
(Fig. 2C). Alternation is the inevitable outcome of such a system (Osborn,
1974b). However, for the following reasons a further proviso is necessary.
If the inhibiting zones, although spherical, had irregular sizes the newly
initiated teeth would be irregularly spaced and alternation could readily be
lost. Since the teeth are regularly spaced it follows that the inhibitory
zones, if they exist, must have equivalent regular sizes. In a larger animal
the teeth are larger and therefore their centres are further apart. It follows
that the inhibitory zones must be larger. Only with the proviso that there
is a smooth gradient in the sizes of inhibitory zones, both in time and
along the length of the jaw, is alternation inevitable.
If the above suggestions are accepted the only dental units which have
an objective reality are individual teeth and the dentition as a whole
(Fig. 2C). Units such as Zuhnreihen, tooth families, and replacement waves
(Fig. 2B) are subjective because they are selected by the observer to
222
J. W. OSBORN
describe the arrangement of teeth; several other types of row can be
selected by connecting different points together (Osborn, 1970: De Mar,
1973). All of them have one feature in common: they describe alternation.
The pattern of aternation has an objective reality.
I t is clear that replacement waves have no influence on the ontogeny of
a dentition: they are the result of the ontogeny. The’ above argument
suggests that Zuhnreihen and tooth families have no more importance in
the ontogeny of alternation than do replacement waves: just as the
inhibitory zones lead to the appearance of Zuhnreihen, so they lead to the
appearance of tooth families. However, once the deciduous teeth in
mammals have been initiated they become separated by bony partitions. I t
is therefore probably no longer possible for the inhibitory influence of a
developing successional tooth to spread through the bony partition and
temporarily inhibit the development of adjacent teeth. Only a deciduous
tooth can inhibit the initiation of its successor. Together they can be said
to comprise a tooth family which therefore has an objective reality in
mammals; and also in mammal-like reptiles such as Dzademodon and
Thrinuxodon although they had more replacement teeth.
THE RELATIONSHIP BETWEEN PATTERNS
Edmund’s (1960) theory of developmental control suggests that the
Zuhnreihe ‘is a constant feature of vertebrate embryology and a basic unit
from which every dentition is built up’ (Cooper e t d.. 1970). If this is
true it should be possible to analyse all dentitions in terms of Zuhnreihen
or of units which might develop due to a modification of the Zahnreihe
control.
The essence of a Zuhnreihe is that it is a row of teeth developed in
sequence from the front to the back of the jaw. By siting the origin of a
Zahnreihe anywhere along the jaws it is possible to account for the
development of any dentition. For example, Osborn (1970)accounted for
the dentition of the insectivore, Tupuia, by means of five Zahnreihen, two
of which started at the front of the jaw. The remaining three started at
the positions of the deciduous canine, third molar, and fourth molar.
Hopson (1971) accounted for the dentition of Diudemodon by means of
two fixed loci for generating Zahnreihen which caused the development of
precanines and canines respectively; and in addition, a locus which moved
through the postcanine region. This moving locus initiated a new Zuhnreihe
whenever it reached a new tooth position. Each new Zahnreihe then
initiated a stimulus which passed back and caused the development of five
teeth in sequence. The model is a little complicated.
Although the Zahnreihe theory of development has a certain elegance it
is not as biologically simple as it might seem to be at first sight. The
following questions need to be answered; where and how does the
Zahnreihe stimulus start; how is the rhythmic initiation of Zuhnreihe
stimuli controlled; what is the nature of the stimulus and how is it
propagated through the jaw; what is the ature of the receptor at each tooth
position which reacts to the Zahnreihe st. nulus; and how are the positions of
these receptors specified?
PATTERNS IN DENTITIONS
Figure 3. Inhibition model applied to tooth development in L. vivlpara The dentition is
generated by a clone of cells (stippled) all of which are capable of forming teeth. A first tooth
(black) is initiated in the clone (A) and is surrounded by a zone in which the initiation of a new
tooth is temporarily inhibited. When the growing anterior margin of the clone has escaped the
inhibition a new tooth is initiated (B and C). Due to interstitial growth these teeth become
separated and new teeth develop between when sufficient space has been created (D). The new
teeth are now surrounded by inhibitory zones. There is no further interstitial growth. Behind
the 'black tooth' new teeth are initiated in sequence whenever the margin of the clone escapes
the inhibitory zone. These zones inexorably force a pattern of alternation on the developing
dentition.
223
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J. W. OSBORN
While the Zuhnreihe control is used to account for the development of
an alternating pattern in the Zahnreihe model, growth and inhibition are
used in the inhibition model. At its simplest, a small colony of cells is
supposed to generate the whole dentition (stippled region in Fig. 3A). The
subsequent growth of the dentition in a lizard, Lacertu vivipura, is illustrated in Fig. 3 (after Osborn, 1971). It will be noted that the sequence
in which teeth are’ generated can be accounted for in terms of growth
represented by spread of the stippled region, and inhibition represented by
the interrupted circles. The picture is complicated by the fact that the
first teeth to be developed anteriorly (identified by dots) are spread apart
due to interstitial growth. This can be verified in Osborn’s (1971) reconstructions of embryo dentitions. When these teeth have become sufficiently
separated (Fig. 3C,D), new teeth are initiated between them. Behind the
first tooth to appear (black tooth), new teeth are initiated in succession.
The sequence in which the first lower teeth are initiated in L. vivipura
is shown in Fig. 4A. In the upper jaw of reptiles the wave replacement of
alternate teeth is disrupted at the premaxillary/maxillary suture (Edmund,
1960; Cooper, 1963). This can be accounted for by suggesting that
different colonies generate the maxillary and premaxillary teeth (Fig. 4B).
Three colonies are needed to account for the pattern of tooth replacement
in Thrinuxodon (Fig. 4C) and initiation in mammals (Fig. 4D); one each
for the incisors, canines, and postcanines (Osborn, 1977). Alternation does
not develop in mammals, probably because the bony crypts separating
adjacent deciduous teeth prevent the spread of inhibition. The deciduous
incisors develop in sequence from front to back because the incisor colony
grows backwards by interstitial growth between the developing first incisor
and canine (Osborn, 1973). The deciduous molars develop in sequence
from back to front because the molar colony grows forwards by interstitial
growth between the developing deciduous molar and canine. The permanent molars develop posteriorly in sequence by backward growth of the
molar colony from the fourth deciduous molar. Interestingly, the directions
in which each colony grows match the gradients in the sizes of teeth.
Furthermore, in an evolutionary sequence, teeth are always lost from the
margins of colonies (Osborn, 1977).
The above suggestions, most of which are merely observations, do not
account for the biological control of growth, but it can scarcely be denied
that such controls are necessary for the development of all metazoans. The
dentition is merely a specific example of a well-known general principle.
The biological control of the temporary zone of inhibition surrounding a
developing tooth is not difficult t o visualize and is discussed by Osborn (1971).
The following example illustrates the way in which the two models,
Zuhnreihe and inhibition, can be used to analyse the development and
organization of an unusual dentition.
Cuptorhinomorphs
Recently Bolt & De Mar (1975) have described and analysed numerous
specimens of Cuptorhinus uguti, a Lower Permian cotylosaur. The captorhinomorphs are interesting reptiles because their polyphyodont dentitions appear to
PATTERNS IN DENTITIONS
A
u
-
Figure 4. A. The pattern of development and tooth replacement in the lower jaw of a reptile
suggests that the dentition develops from a single colony of cells. B. In the upper jaws the
alternating pattern is broken at the premaxillary/maxillary suture suggesting that two colonies
are involved. D. Three colonies contribute to the mammalian dentition. C. Tltrinaxodon, a
mammal-like reptile, was polyphyodont and heterodont. The pattern of tooth replacement is
broken at the same positions as the pattern of tooth development in mammals. This suggests
that the dentition of Tltrinaxodon also developed from three cell colonies. The shaded teeth
(apart from those in C) are the first teeth to develop in their respective colonies. The same may
have been true for the cross-hatched teeth in C. The arrows indicate the directions in which the
colonies grow during development.
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J. W. OSBORN
226
contain Zahnreihen but do not obviously show a pattern of alternation. A good
example is Lubidosuurikos bakeri (Fig. 5A) described by Edmund (1960). Bolt
& De Mar concluded that in these types of dentition some form of biological
control led to the development of Zahnreihen without the concomitant
epiphenomenon of tooth families which are a requirement of the inhibition
model. However, with the exception of a ‘tusk’at the front of the dentition a
regular pattern of alternation is revealed by the lines shown in Fig. 5B. These
lines suggest that instead of growing perpendicular to the jaw axis, as in all the
animals described above, the colony of cells responsible for the dentition of
Labidosaurikos grew posteriorly and palatally (in the directions of the arrows
which identify tooth families). It might be possible to test this suggestion by
studying growth lines in the bone of sectioned material.
Palatal
. _ _ -
---
A
A
=
-
-
B
Figure 5. The upper dentition and jaw of Lobidosvrurikos baked (after Edmund. 1960).
Zahnreihen are indicated in A and alternation is indicated in B. The arrows in B indicate the
probable directions in which the jaw grew-and also join together units comparable to tooth
families.
The fewer teeth a dentition contains the easier it is to fit into a
developmental pattern. For example, it can easily be visualized that a single
row of unreplaced teeth fits both the Zuhnreihe pattern and the inhibition
pattern. The more teeth a dentition contains the more restraints it places on a
theory of developmental controls. For this reason I have selected for analysis
the two most complex dentitions described by Bolt & De Mar (1975). Their
analyses in terms of Zuhnreihen are shown in Fig. 6A,C. Analyses in terms of
alternation (inhibitory control) are shown in Fig. 6B,D.
For Bolt & De Mar (1975) each Zahnreihen originally started at the front of
the jaw. Thus, at a rough calculation, about 20 teeth have been lost from the
front of each Zahnreihe indicated by the letter Z and many teeth have been
lost from the other Zuhnreihen (w, x and y), the number depending on the
PATTERNS IN DENTITIONS
227
palatal
anterior
lingual
anterior
D
lingual
Figure 6. The most complex upper (A) and lower ( C ) dentitions figured by Bolt & De Mar (1975).
The lines connect the Zahnreihen recognized by these authors. B and D demonstrate alternation
in the same dentitions. The alternation in terms of its development is shown in Fig. 7.
distance of the anterior end of each remaining row of teeth from the front of
the jaw. To account for the lost teeth they offered two suggestions. First, the
teeth drifted buccally and were shed from the outer edge of the jaw (cf.
Batoidea described above). Second, the jaws were pushed apart by growth at
sutures between the tooth bearing bone, the dentary, and adjacent bones. New
bone was added lingually to accommodate new teeth, and old bone was
removed buccally together with the teeth it supported. The latter seems more
probable because it is very difficult to visualize how ankylosed teeth could drift
through the jaw.
A diagram, exaggerated for simplicity, of my interpretation of a developing
captorhinomorph dentition is shown in Fig. 7. The cell colony responsible for
tooth initiation and development grew almost vertically anteriorly as in nearly
all animals, but it grew lingually (and posteriorly) in the rest of the jaw, as in
Batoidea. Thus, the alternating pattern was edge on to the jaw anteriorly with
J. W. OSBORN
228
the result that teeth tended to be replaced from below and only a single row of
teeth is present. Posteriorly, the alternating pattern was spread over the jaw
with the result that old teeth were not often replaced from below, but instead
new teeth were added to the lingual side of the dentition to produce a tooth
battery which was most marked in Lubidosuurikos (Fig. 5).
-
Anterior
Figure 7. In the ancestor to captorhinomorphs the alternating pattern was vertical (Fig. 2E).
During evolution the posterior end of the pattern was twisted to lie over the surface of the jaw
(cf. Fig. 2D). This diagram suggests the relationship between the anterior vertical pattern and
the posterior twisted pattern. The black circles are functioning teeth, the open circles are either
lost or as yet undeveloped teeth. A single row of teeth functions anteriorly and blends with a
battery posteriorly. Zahnrellte lines would run diagonally from top left to bottom right. The
single row of teeth at the front would belong to two or three different Zahnreihen (cf. Bolt &
De Mar’s interpretation of a single Zahnreihe in Fig. 6A and C).
TESTING THE MODEL
So far, it has not been found possible to devise an experiment to test
whether a newly initiated tooth is surrounded by a zone of tissue in which the
initiation of a new tooth is temporarily inhibited. However, the model predicts
that the whole molar dentition of a mammal develops from a colony of cells
which is initially differentiated in the region of the first molar to develop (the
same is true for the incisor dentition and for the canine). It is not possible to
identify the colony until this first molar has been initiated. Andrew Lumsden
in this laboratory has dissected out from 12 day embryo mice the bud of the
first molar tooth and transplanted it into the anterior chamber of the eye of
homologous hosts. Within three weeks perfect crowns of all three molar teeth
(the whole molar dentition) develop and mineralize in this site (Lumsden &
Osborn, 1975). The purity of the transplant is assessed by serially sectioning
control buds dissected from embryos. There is little doubt that the whole
molar dentition in the mouse develops from a small colony of cells which at 12
days is almost entirely represented by the first molar bud.
PATTERNS IN DENTITIONS
229
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