Blackwell Science, LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The
nean Society of London, 2005? 2005
145Issue: ?
523538
Original Article
Lin-
A. MEXICANUS ORAL DENTITIONJ. TRAPANI
ET AL.
Zoological Journal of the Linnean Society, 2005, 145, 523–538. With 12 figures
Ontogenetic transition from unicuspid to multicuspid oral
dentition in a teleost fish: Astyanax mexicanus, the
Mexican tetra (Ostariophysi: Characidae)
JOSH TRAPANI1*, YOSHIYUKI YAMAMOTO2 and DAVID W. STOCK1
1
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309–0334, USA
Evolutionary Anatomy Unit, Department of Anatomy and Developmental Biology, University College
London, Gower Street, London WC1E 6BT, UK
2
Received December 2004; accepted for publication April 2005
Teleost fishes display a remarkable diversity of adult dentitions; this diversity is all the more remarkable in light of
the uniformity of first-generation dentitions. Few studies have quantitatively documented the transition between
generalized first-generation dentitions and specialized adult dentitions in teleosts. We investigated this transition in
the Mexican tetra, Astyanax mexicanus (Characidae), by measuring aspects of the dentition in an ontogenetic series
of individuals from embryos to 160 days old, in addition to adults of unknown age. The first-generation dentition and
its immediate successors consist of small, unicuspid teeth that develop extraosseously. Multicuspid teeth first appear
during the second tooth replacement event, and are derived from single tooth germs, rather than from the fusion of
multiple conical tooth germs. We document that the transition from unicuspid to multicuspid teeth corresponds to
a change in the location of developing tooth germs (from extraosseous to intraosseous) and in patterns of tooth
replacement (from haphazard to simultaneous within a jaw quadrant). In addition, while the size of the largest teeth
scales with positive allometry to fish size, the transition to multicuspid teeth is accompanied by an exceptionally
large increase in tooth size. © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005,
145, 523–538.
ADDITIONAL KEYWORDS: allometry – first-generation dentition – morphology – morphometrics – ontogeny –
teeth – tooth development – tooth replacement.
INTRODUCTION
The teeth of bony fishes display diverse sizes, shapes,
numbers and presence/absence on bones of the oral
jaws and pharyngeal skeleton (e.g. Peyer, 1968; Huysseune & Sire, 1998; Stock, 2001). What is especially
remarkable about this diversity is that it arises from
what appears to be a common ground-state (Sire et al.,
2002; Streelman et al., 2003). The first-generation
teeth of all species for which data exist are small, conical, and – where they have been examined in sufficient detail – lack some of the structural details of
*Corresponding author. Current address: Department of
Paleobiology, National Museum of Natural History,
Smithsonian Institution, NHB, MRC121, Washington, D.C.,
20013-7012, USA. E-mail: [email protected]
their successors (Sire et al., 2002 and references
therein, see also: Berkovitz, 1977; Gosztonyi, 1984;
Govoni, 1987). This characteristic first-generation
dentition is found even in some fish that lack oral
teeth as adults (Huysseune & Sire, 1997b; Kakizawa
& Meenakarn, 2003).
Features of bony fish dentitions often change during
ontogeny (Howes & Sanford, 1987; Nakajima & Yue,
1989, 1995; Hahn, Pavanelli & Okada, 2000; Murray,
2004), and differences within (Roberts, 1974; Meyer,
1990; Caldecutt, Bell & Buckland-Nicks, 2001; Tigano
et al., 2001; Trapani, 2003, 2004) and between
(Parenti & Thomas, 1998; Lewis et al., 1999) taxa
may often track ecological specializations (Sage &
Selander, 1975; Motta, 1989; Blaber, Brewer & Salini,
1994; Kanda & Yamaoka, 1995; Mullaney & Gale,
1996). While teeth in adult fishes have been relatively
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145, 523–538
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J. TRAPANI ET AL.
well-studied (e.g. Peyer, 1968; Huysseune & Sire,
1998), and more attention is now being focused on
first-generation dentitions (Huysseune & Sire, 1997a;
Sire et al., 2002), there is little information about what
happens in between, or how the transitions from generalized first-generation dentitions to more specialized adult dentitions occur.
A related issue involves tooth replacement patterns.
That many lower vertebrates share a regular pattern
of wave-like tooth replacement maintained throughout life (e.g. Edmund, 1960; Berkovitz, 2000) is conventional knowledge. Such a regular pattern makes
sense in terms of organismal fitness; because teeth are
essential for food procurement, a lack of functional
teeth in numerous adjacent positions would be detrimental (Osborn, 1975; Berkovitz, 2000). However, a
perusal of the literature indicates that deviations from
regular patterns of tooth replacement are common in
teleost species. Replacement may be haphazard, likely
reflecting a relaxation of this constraint (e.g. in species
where teeth are extremely closely packed: Govoni,
1987) or may fit a completely different pattern, reflecting specialization. For example, in piranhas (Pygocentrus and Serrasalmus), the teeth in each quadrant of
the jaw interlock to enhance shearing capability, and
are replaced simultaneously (Berkovitz, 1975; Berkovitz & Shellis, 1978). While multiple patterns of tooth
replacement have been described, whether such patterns vary in ontogeny has not been investigated.
In order to address how the transition from generalized first-generation to specialized adult dentitions
occurs, and to document initiation and maintenance of
tooth replacement patterns, we collected data on the
ontogeny of oral dentition of the Mexican tetra, Astyanax mexicanus de Filippi, 1853 (Family Characidae).
The characiforms are one of the most diverse teleost
groups with regard to dentition (e.g. Roberts, 1967,
1969) and adult A. mexicanus possess mainly multicuspid oral teeth, a specialization that has evolved
independently in a number of teleost lineages (Huysseune & Sire, 1998). One potentially unusual feature
of multicuspid characiform teeth is that they have
been hypothesized to result from the fusion of multiple
conical teeth onto a hard base (Roberts, 1967). This
hypothesis, based largely on examination of clearedand-stained specimens, remains to be tested through
more sensitive histological analysis.
Astyanax mexicanus is a popular model organism in
evolutionary developmental biology (e.g. Jeffery, 2001;
Yamamoto et al., 2003; Yamamoto, Stock & Jeffery,
2004), and its population genetics (Dowling, Martasian & Jeffery, 2002) and cranial osteology (ValdezMoreno & Contreras-Baldera, 2003) have also been
recently studied. We characterize the appearance of
the first-generation dentition in this species, estimate
number and timing of subsequent tooth generations.
We look at sectioned tooth germs to determine
whether or not multicuspid teeth in A. mexicanus are
truly compound elements. These data serve to document the changes associated with the ontogenetic
transition from unicuspid to multicuspid oral teeth in
this species.
MATERIAL AND METHODS
ANIMALS
Adult individuals of A. mexicanus were obtained from
the laboratory of W.R. Jeffrey (University of Maryland) and maintained at the University of Colorado;
these fish are derived from collections made from wild
populations at Balmorhea State Park, Texas (Strickler, Yamamoto & Jeffery, 2001). Astyanax mexicanus
includes both surface and cave forms; for this study we
examined only the former. After spawning, embryos
were raised at 25 °C for several weeks, then at ambient laboratory temperature ( ≈ 22–24 °C) thereafter.
They were kept first in plastic beakers at controlled
temperature, then transferred to finger-bowls, and
finally pooled into a 38-litre fish tank. Fish were fed
each day on brine shrimp and/or commercial flake
food, and generally appeared active and healthy
throughout the course of the study. Our sample
included numerous embryonic fish (< 5 days postfertilization: dpf), a series of 109 fish ranging from 5 to
163 dpf, and an additional 11 fish representing fully
mature individuals of unknown age. Generation time
in A. mexicanus is 3–6 months (Jeffery, 2001), so our
sample encompasses most of the time between first
appearance of teeth and onset of sexual maturity.
CLEARING-AND-STAINING,
MICROSCOPY
Fish were fixed overnight in 4% paraformaldehyde,
macerated in trypsin/sodium borate solution, stained
with Alizarin Red S, and cleared with potassium
hydroxide and glycerol, largely following the clearingand-staining procedure outlined in Taylor (1967).
Smaller individuals were examined with an inverted
compound microscope; larger individuals were examined under a dissecting scope.
Individuals younger than 30 dpf were examined
without clearing-and-staining using Nomarski DIC
optics. Embedding in 4% methyl cellulose kept fish
stationary during observation without harm; although
this allowed the potential for repeated observations of
the same individuals, we did not take care to choose
the same individuals for multiple observations. Embedding in 2% agarose was also satisfactory for
observation, but usually fatal. We examined both live
and cleared-and-stained fish within this age range to
test consistency of observations.
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145, 523–538
A. MEXICANUS ORAL DENTITION
SECTIONING
Fish were fixed in Bouin’s solution (Sigma) for one to
several days at room temperature, then washed in
70% EtOH until the solution became clear. Next, samples were dehydrated in a graded methanol series and
placed in xylene. The samples were then embedded in
paraffin and sectioned at 10 µm. Finally, sections were
deparaffinized and stained with haematoxylin and
eosin.
MEASUREMENTS
AND ANALYSIS
For each fish, we recorded the age in days (when
known) and total length (TL, measured to the nearest
0.1 mm with calipers prior to fixation). Size of fish at a
given age is dependent upon several factors, including
water temperature, amount and quality of food, size of
tank, and number of individuals per unit space. However, there is a strong relationship between age and
TL (R2 = 0.9516, P = 3.56 × 10−72, N = 109) for our
sample.
We counted the total number of teeth on the premaxillaries and lower jaws (maxillary teeth were considered separately), noted how many were unicuspid
or multicuspid, and also counted total number of
cusps. This method allowed us to summarize cusps in
each individual with a single ratio (total number of
cusps/total number of teeth), even though this number
is not always an integer. For the first-generation dentitions, order of appearance was determined both by
noting how tooth numbers changed each day and by
matching teeth based on their relative positions, as
well as by looking for signs of new teeth (e.g. incompletely mineralized or unattached tooth caps). We also
looked for signs of tooth replacement throughout the
series.
For photography, embedded fish were orientated
face-down on slide coverslips on an inverted compound
scope mounted with a digital camera. Cleared-andstained specimens were held in position in a small
plastic cylinder filled with glycerol to prevent movement and to standardize orientation under a dissecting scope also mounted with a digital camera. Gums
were peeled away in older, cleared-and-stained specimens. All fish were photographed in rostral view (i.e.
snout pointing at camera), and tooth heights measured (as linear distances in pixels from base to cap)
from images using tpsDig version 1.40 (by F.J. Rohlf –
available at http://life.bio.sunysb.edu/morph/); pixels
were converted to millimetres in Microsoft Excel. A
total of 589 teeth (including 327 premaxillary teeth
and 262 dentary teeth) were measured in this fashion.
Although we measured as many teeth as were visible,
the orientation of the images and the relative sizes of
the teeth bias the sample toward the (usually larger)
teeth located rostrally; however, this is not problem-
525
atic for our interpretations because we were most
interested in these teeth. Adult fish of unknown age
were not photographed. Statistical analyses were performed with the freeware PAST (Hammer, Harper &
Ryan, 2001) and SPSS v.12.0.
RESULTS
APPEARANCE
OF FIRST-GENERATION DENTITION
Tooth germs in A. mexicanus are visible in histological
sections stained with toluidine blue at between 3 and
4 dpf (D.W. Stock, unpubl. data). Their position (one in
each jaw quadrant) is consistent with observations of
teeth in living individuals, which are visible by 108 h
post-fertilization (hpf; Fig. 1A). A second tooth (rostral
to the first on the premaxillaries and caudal to it on
the lower jaws) becomes visible in each quadrant by
132 hpf. By 8 dpf, a third tooth has appeared caudal to
the first on the premaxillaries, and rostral on the dentaries. The appearance of this third tooth is rapidly
followed by a fourth on the dentary, caudal to all the
others. These first teeth are fairly widely spread out;
subsequent teeth appear to fill in positions rostral to,
caudal to, and between them.
The order of appearance of the first-generation dentition is summarized in Figure 2 for one side of the jaw.
Teeth do not appear in a regular pattern in either time
or space, nor is there consistency between premaxillary and lower jaws. However, while we examined
several fish each day, as well as fish from different
spawning events, and while there was a small amount
of variability between sides of a single fish as well as
between individuals (the latter likely due to differences in TL), the order of appearance and location
of first-generation teeth remained consistent. By 35–
40 dpf (≈ 10 mm TL), the full complement of ≈ 40 firstgeneration teeth (≈ 10 per quadrant) was visible
(Fig. 1D).
NUMBER
OF TOOTH GENERATIONS AND
CORRESPONDING CHANGES IN THE DENTITION
Both first-generation teeth and their immediate successors were conical and developed extraosseously
(Fig. 3); thus, it was sometimes difficult to distinguish
replacement from first-generation teeth. Our analysis
of tooth heights (see below) indicates that replacement
begins at around 25 dpf, by which time most firstgeneration teeth were visible (6–7 on each premaxilla,
8 on each lower jaw). It is notable that this corresponds to the time that both rostral-most and caudalmost teeth in the tooth row were present (Fig. 2B–C).
Other morphological signs of replacement (e.g. resorption of bone around tooth bases, new teeth appearing
very close to existing functional teeth) became com-
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145, 523–538
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J. TRAPANI ET AL.
A
B
P
P
*
*
*
*
M
*
*
C
D
P
P
*
* *
*
*
** ***
* *
* *
*
*
Figure 1. First-generation dentition in Astyanax mexicanus. Asterisks indicate positions of teeth. A, 5 days postfertilization (dpf) (4.5 mm total length (TL, measured to the nearest 0.1 mm with calipers prior to fixation)) showing one
tooth on each jaw quadrant, left side. M, Meckel’s cartilage; P, premaxilla. B, 10 dpf (5.2 mm TL) showing three teeth on the
right premaxilla; one tooth is also visible on the lower jaw. C, 28 dpf (7.8 mm TL) showing five attached teeth, and one unattached, on the right premaxilla. D, 40 dpf (9.2 mm TL) showing signs of resorption (left arrow) and replacement by a second
generation of unicuspid teeth (right arrow) on the left premaxilla. Scale bars = 100 µm.
mon around 35 dpf. Replacement of first-generation
teeth was random, and did not correspond to initial
order of appearance.
We attempted to determine the number of tooth
replacement cycles individuals underwent during the
course of this study by measuring tooth heights from
the series of fish of known age. Analysis of variance
indicates that premaxillary and lower jaw teeth do not
differ significantly in heights, controlling for either
age (F = 1.535; P = 0.218) or TL (F = 3.229; P = 0.076)
of fish, and we pooled teeth measured from both premaxillaries and dentaries in subsequent analyses. A
plot of all tooth heights against age (Fig. 4A) or log TL
(Fig. 4B) shows step-like increases that match well
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145, 523–538
A. MEXICANUS ORAL DENTITION
527
A
P
2 9
48 8 1
3
R
7 3
5 1
10 6
5 2 4 9 6 10
7
C
LJ
B
1
X
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C
2
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3
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4
X
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5
6
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X
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7
X
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X
8
X
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9
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10
X
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Premaxilla
1
X
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2
3
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X
X
7
8
X
X
X
X
X
X
X
9
10
X
X
X
X
X
Lower Jaw
Figure 2. Order of appearance of the first-generation dentition on one half (right) of the jaw in Astyanax mexicanus. A,
schematic of the premaxillary and lower jaw. Order is indicated by numbers. B, graph of tooth appearance patterns on the
premaxilla. Numbers represent tooth positions and time runs vertically down. C, graph of tooth appearance patterns on the
lower jaw. Abbreviations: P, premaxilla; LJ, lower jaw, C, caudal; R, rostral.
with the morphological indications of tooth replacement (discussed below). Histograms of the frequency
of all tooth heights (Fig. 5A) or maximum tooth
heights for each individual (Fig. 5B) show four separate peaks, which match with plateaus in Figure 4 and
that we interpret as corresponding to four tooth generations, and thus three replacement cycles.
Tooth numbers and the proportions of unicuspid and
multicuspid teeth change in concert with these cycles.
Total number of teeth (Figs 6A, 7A) first increases as
first-generation teeth appear, reaching a plateau of
≈ 40 teeth. Tooth numbers then remain approximately
constant through the next tooth generation, also consisting of conical teeth that develop extraosseously.
At about 75 dpf (≈ 17 mm TL), another tooth replacement cycle begins, with the rostral-most two teeth (i.e.
those closest to the symphysis) in each jaw quadrant
replaced by bi- or tricuspid teeth. These teeth develop
intraosseously, either in crypts on the lingual side of
the bone (premaxillary) or within it (lower jaw).
Premaxillary teeth also develop with cusps pointing
lingually, and must rotate into functional position.
Rotation appears to occur in soft epithelial tissue,
followed by mineralization of the tooth base, which
eventually joins with remodelled bone.
After ≈ 75 dpf, the total number of unicuspid teeth
begins to decline, with a concomitant increase in the
number of multicuspid teeth (Figs 6B, 7B). A plot of
the number of unicuspid against number of multicuspid teeth shows a strong negative relationship ( R2 =
−0.8508, P = 8.48 × 10−20, N = 46 as we only included
fish with at least one multicuspid tooth), with a
reduced major-axis regression slope of −1.05 (upper
and lower 95% confidence intervals are −0.91 and
−1.16, respectively), indicating overall 1 : 1 replacement. However, there is variability underlying this
overall pattern, and it appears that total tooth numbers decrease after 75 dpf, and then later increase.
This later increase reflects the number of small, unicuspid teeth in the caudal-most portion of the lower jaws.
CHANGES
IN NUMBERS OF CUSPS
Total number of cusps (summed over all teeth)
increases only slightly (Figs 6C, 7C) from ≈ 75 dpf until
the next tooth replacement cycle at around 120 dpf
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145, 523–538
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J. TRAPANI ET AL.
(≈ 28 mm TL). In this cycle, unicuspid teeth continue to
be replaced by multicuspid teeth, with only teeth on
the caudal portions of the lower jaws unaffected. Preexisting multicuspid teeth are replaced by successors
that generally possess more cusps (from 4 to 6). Premaxillaries now have two rows of teeth. Also, by this
point, teeth are undergoing simultaneous (or nearly
simultaneous) replacement within a quadrant, accompanied by large-scale bone resorption. However, the
caudalmost few teeth on each side of the lower jaw
are an exception; successors continue to develop
extraosseously and replacement does not appear to follow a regular pattern. Nor does replacement of these
teeth appear to be coordinated with replacement of
multicuspid teeth on the same quadrant.
After the appearance of multicuspid teeth in
A. mexicanus, the dentition (examples shown in
Fig. 8) remains relatively stable in terms of tooth
numbers; variability results from addition of small,
usually unicuspid teeth on the caudal portion of the
lower jaw. However, the total number of cusps continues to increase; although not a strictly linear increase,
it still shows a strong linear relationship with both log
TL (R2 = 0.8321, P = 3.27 × 10−45, N = 114) and age
(R2 = 0.9070, P = 6.75 × 10−54, N = 103). In addition,
the number of cusps per tooth (total number of cusps
divided by total number of teeth) increases with
respect to log TL and age (Fig. 9); there is also a very
strong relationship between the number of multicuspid teeth and the number of cusps per tooth
(R2 = 0.9750, P = 1.32 × 10−91, N = 114).
A
B
Figure 3. Sections through first (A, one month) and second (B, two months) generation oral teeth in Astyanax
mexicanus. Scale bars = 50 µm.
Log tooth height (mm)
0
MAXILLARY
TEETH
Maxillary teeth first appear in fish at about 100 days
of age (≈ 28 mm TL); this does not correspond closely
A
B
-0.5
-1
Premaxillary teeth
Lower jaw teeth
-1.5
-2
0
25
50
75
100
Age (days)
125
150
175
0.5
0.75
1
1.25
1.5
1.75
Log TL (mm)
Figure 4. Tooth heights as a function of A, age in days; B, log total length (TL) in mm. Arrows indicate plateaus corresponding to tooth replacement events.
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145, 523–538
A. MEXICANUS ORAL DENTITION
A
10
8
A
40
35
30
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20
15
10
5
0
50
6
B
45
Number of teeth
Frequency
50
45
Number of teeth
12
529
4
2
Unicuspid teeth
Multicuspid teeth
40
35
30
25
20
15
10
5
0
140
50
B
Frequency
40
Number of cusps
0
C
120
100
80
60
40
20
0
0
30
25
50
75
100
125
150
175
Age (days)
Figure 6. Features of the dentition of Astyanax mexicanus
as a function of age in days. A, total number of teeth. B,
numbers of unicuspid and multicuspid teeth. C, total number of cusps.
20
10
0
-2.00 -1.75 -1.50 -1.25 -1.00 -0.75 -0.50 -0.25 0.00
Log tooth height (mm)
Figure 5. Frequency distributions of tooth heights.
Arrows indicate peaks corresponding to tooth replacement
events, and to the plateaux in Fig. 3. A, only the single tallest tooth from each dentigerous bone. B, all measured
teeth.
with tooth replacement events on the lower jaw and
premaxillaries (as shown in Fig. 4). The first teeth to
appear are conical; subsequently, teeth with 3–6 cusps
appear. Teeth appear to develop behind the maxillary
bone, with cusps facing 180° from functional position.
Individuals may have 0–2 teeth on each maxillary
bone, matching the description of Valdez-Moreno &
Contreras-Baldera (2003), but deviating from the
number of maxillary teeth seen in many cavefish
populations (Yamamoto et al., 2003). The relationship
between number of maxillary teeth and log TL is
weak but significant (R2 = 0.1460, P = 0.028, N = 33),
whereas the relationships between number of maxillary teeth and age is not (P = 0.113, N = 22). This is
also true of the relationships between number of maxillary cusps and log TL (R2 = 0.5134, P = 2.74 × 10−6,
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145, 523–538
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J. TRAPANI ET AL.
50
A
Number of teeth
45
A
40
35
30
25
20
15
10
5
Number of teeth
0
50
B
45
Unicuspid teeth
Multicuspid teeth
40
35
30
25
20
15
B
10
5
0
Number of cusps
180
C
160
140
*
120
100
80
60
40
20
0
0.5
0.75
1
1.25
1.5
1.75
2
Log TL (mm)
Figure 7. Features of the dentition of Astyanax mexicanus
as a function of log total length (TL) in mm. A, total number
of teeth. B, numbers of unicuspid and multicuspid teeth. C,
total number of cusps.
N = 33) and age (P = 0.056, N = 22). The number of
cusps per maxillary tooth has relatively weak but significant relationships with both log TL (R2 = 0.5708,
P = 5.79 × 10−7, N = 33) and age (R2 = 0.2782, P =
0.014, N = 22).
SCALING
OF VARIABLES
Our analysis of the number of tooth generations
within the range of ages and sizes in the series of fish
we studied is predicated on the assumption that successor teeth are larger than the functional teeth they
replace. This assumption is borne out by the data
(Figs 4, 5) and allows us to ask how much larger each
Figure 8. Transitional and adult dentitions in Astyanax
mexicanus. A, live fish – 65 days post-fertilization (dpf)
(16.9 mm total length (TL)) showing premaxilla, with the
first multicuspid teeth developing prior to replacing conical
predecessors. Scale bar = 100 µm. B, cleared-and-stained
fish – 163 dpf (41.8 mm TL). Asterisk indicates maxillary
tooth. Scale bar = 1 mm.
successive tooth generation is, and how the timing of
tooth replacement events scales with fish size and age.
The relationship between log maximum tooth height
and log TL (pooling premaxillary and lower jaw teeth)
is strong and significant (R2 = 0.9626, P = 4.89 × 10−71,
N = 99). A reduced major-axis regression analysis of
these variables has a slope of 1.74 (1.68 and 1.81 are
lower and upper 95% confidence limits, respectively),
indicating positive allometry; i.e. teeth are relatively
bigger in larger fish.
Figure 10 shows the age (Fig. 10A), size (Fig. 10B),
and corresponding maximum tooth heights (Fig. 10C)
of each of the four tooth generations described in this
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145, 523–538
A. MEXICANUS ORAL DENTITION
# cusps/tooth
5
A
531
B
4
3
2
1
0
25
50
75
100
125
150
175 0.5
0.75
Age (days)
1
1.25
1.5
1.75
2
Log TL (mm)
Figure 9. Number of cusps per tooth (calculated as total number of cusps/total number of teeth) as a function of age in days
(A) and log total length (TL) in mm (B).
Age (days)
140
120
paper. Each of these reflects an average, because there
was variability between individuals, but corresponds
closely to the patterns illustrated in Figures 4 and 5.
In Figure 11, we show time, TL and tooth height differences in fish between the onsets of successive tooth
generations. Approximately 20 days elapses between
the first appearance of teeth and the first appearance
of replacement teeth, whereas approximately 50 days
elapses between each of the succeeding two tooth generations (Fig. 11A). Increases in fish TL are similar
between the first and second, and third and fourth
tooth generations, but are larger between the second
and third (Fig. 11B).
The largest teeth in the second tooth generation are
approximately twice the size (in terms of height) as
the largest teeth in the first (Fig. 11C). It is notable
that the third tooth generation, in which the first
multicuspid teeth appear, shows largest teeth five
times the size of the largest unicuspid teeth that preceded them. Successor multicuspid teeth are about 2.5
times the size of their multicuspid predecessors.
A
100
80
60
40
20
0
40
B
TL (mm)
30
20
10
Tooth height (mm)
0
1
C
FORMATION OF
0.75
0.5
0.25
0
1
2
3
4
Tooth generation
Figure 10. Age in days (A), total length (TL) in mm (B)
and maximum tooth height in mm (C) at the onset of tooth
generations 1–4.
MULTICUSPID TEETH IN
A. MEXICANUS
Sections through the oral jaws in 3-month-old
A. mexicanus show that teeth represent single, rather
than compound, elements (Fig. 12). Developing tooth
germs are few and highly discrete, rather than more
numerous and close together as would be expected if
multicuspid teeth were composed of fused conical
teeth. In addition, developing tooth germs, regardless
of stage, possess single pulp cavities lined with
odontoblasts (dentine-forming cells). Cusps in both
developing and functional teeth appear reflective of
differential deposition of enameloid and/or dentine.
Support for this idea can be seen in the orientation
of odontoblast processes (dentinal tubules) in the
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145, 523–538
532
J. TRAPANI ET AL.
60
A
Time (days)
50
40
30
20
10
0
-fold increase in TL
3
B
2.54
2.5
2
1.78
1.59
1.5
1
0.5
0
-fold increase in
tooth height
6
C
5.01
5
4
3
2.51
1.97
2
1
0
1 and 2
2 and 3
3 and 4
Tooth generations
Figure 11. Differences between successive tooth generations in terms of time (A), increase in fish total length (TL)
(B) and increase in tooth height (C).
dentine, which are consistent with the existence of a
single pulp cavity throughout the development of the
tooth, rather than the closure or fusion of smaller pulp
cavities from separate elements. Further support for
the singular nature of these teeth is the continuous
dentine–predentine junction documented in both
developing and functional teeth.
other species (Sire et al., 2002). We did not investigate
the microstructure of the dentine, or the nature of the
pulp cavity, to see whether they match precisely with
the Type I first-generation teeth proposed by Sire et al.
(2002) as characteristic of actinopterygians, but the
small size of these teeth alone precludes their being
unduly complex.
Despite morphological and structural similarities
between first-generation teeth in different species, the
order of appearance of these teeth is not identical.
In species for which data are available, including
A. mexicanus, the first oral tooth to appear in each jaw
quadrant is usually soon flanked by two others; however, conservation does not appear to extend beyond
this stage. In some species, such as the rainbow trout
Salmo gairdneri (= Oncorhynchus mykiss: Behnke,
1992) (Berkovitz, 1977, 1978) and the cichlids Hemichromis bimaculatus and Astatotilapia (= Haplochromis: van Oijen et al., 1991) burtoni (Huysseune, 1990),
first-generation tooth germs continue to appear in a
fairly regular, often alternating pattern. In other species, including three armoured catfish (Corydoras
aeneus, C. arcuatus and Hoplosternum littorale) studied by Huysseune & Sire (1997b) and A. mexicanus
(this study), there is no regular pattern of appearance.
It is also possible that the lack of regular pattern indicates that, as in cyprinid (Nakajima, 1984; Huysseune, Van der Heyden & Sire, 1998) pharyngeal teeth,
some of these ‘first-generation’ teeth are actually
replacement teeth that are cofunctional with their
predecessors. Serial sections would be necessary to
test this possibility.
The first-generation dentition in this species takes
about 35–40 days to appear. As in all other teleosts,
these teeth develop in the epithelial tissue outside
the bone to which they will attach (Trapani, 2001).
Although we did not discern any regular pattern to
their appearance, and although paired bones within
an individual may be slightly out-of-phase with one
another (as may be individuals of a given age), firstgeneration teeth in A. mexicanus do develop in a definite order (Fig. 1), which held true with little variation for all the individuals examined in this study,
including the products of different parents and spawning events.
TOOTH
DISCUSSION
FIRST-GENERATION
DENTITION
In A. mexicanus, as in other species of characiforms
(Roberts, 1967; Lawson & Manly, 1973; dos Santos &
Godinho, 2002) and actinopterygians generally (Sire
et al., 2002), first-generation teeth are conical. They
are also small (< 40 µm), matching observations in
REPLACEMENT
There is a surprising paucity of data on the number
and timing of tooth replacement events in the oral
jaws of teleosts; where these data are available, they
come in a variety of different forms. Streelman et al.
(2003) reported that unicuspid first-generation teeth
are replaced by bi- or tricuspid successors at 17 days
in Labeotropheus fuelleborni and at 42 days in Metriaclima zebra; these fish are both Lake Malawi cichlids.
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145, 523–538
A. MEXICANUS ORAL DENTITION
A
533
B
FT
FT
Od
D
PC
RT
C
D
Figure 12. Multicuspid teeth in Astyanax mexicanus; sections through a 3-month individual. A, functional teeth (FT) and
developing replacement tooth (RT) on the dentary (D). Scale bar = 100 µm. B, close-up of functional tooth showing odontoblasts (Od) grouped on the edge of the pulp cavity (PC); the paths of odontoblast process (dentinal tubules) through the
dentine is apparent. Scale bar = 50 µm C, close-up of developing tooth germ, showing a single pulp cavity lined with odontoblasts as well as a continuous dentine-predentine junction (black arrows). Scale bar = 50 µm. D, section through another
functional tooth, showing the continuous nature of the dentine-predentine junction (black arrows). Scale bar = 50 µm.
Steyn et al. (1996) reported that teeth had been
replaced at least once by the age of 45 days posthatching in Hydrocynus raised in the laboratory (TL of
≈ 40 mm). In A. mexicanus, we estimate that tooth
replacement begins at around 25 days.
Berkovitz & Moore (1974) conducted a longitudinal
study of tooth replacement in the rainbow trout Oncorhynchus mykiss, finding that teeth remained functional anywhere from eight to 16 weeks. Gagiano,
Steyn & du Preez (1996) monitored three Hydrocynus
individuals for six months, noting that two replaced
their teeth twice during this period, while the last
underwent three replacements. Further estimates
come from Berkovitz & Shellis (1978), who examined
tooth replacement in piranhas and estimated approximately 27 replacement events over a fish’s lifetime.
We have documented four tooth generations and three
replacement events during 163 days of study. Tooth
replacement is expected to slow with increasing size
and age (Huysseune & Sire, 1998), but a rough extrapolation of our data over the lifetime of A. mexicanus
(estimated at around 6 years by aquarists) leads to an
estimate of around 40 lifetime replacement events.
Haphazard replacement, as seen in young
A. mexicanus, is not unique to this species; it was
observed commonly in characiforms with conical teeth
by Roberts (1967). He also noted that simultaneous
replacement of all teeth in a jaw quadrant was
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145, 523–538
534
J. TRAPANI ET AL.
common in characids with multicuspid teeth,
although in many cases replacement appeared independent between quadrants (Roberts, 1967). One
taxon that deviates from these observations is Hydrocynus. Adults of this genus have conical teeth (Brewster, 1986) that form in separate bony compartments
(Eastman, 1917), and many observations indicate
that this fish replaces its entire dentition (all quadrants) at once (Begg, 1972; Gaigher, 1975; Tweddle,
1982; Gagiano et al., 1996). These features, plus the
appearance of tricuspid teeth at an earlier stage, are
thought to indicate that adult dental features in this
genus are secondarily derived (Roberts, 1967; Brewster, 1986).
Given that A. mexicanus at no time exhibits the
wave-like replacement pattern considered typical of
lower vertebrates, we sought to assess how common
deviations from this pattern are within the oral
dentitions of teleosts by investigating the literature
addressing patterns of tooth replacement. Regular
patterns of replacement were discerned in the trout
Oncorhynchus mykiss (Berkovitz & Moore, 1975;
Berkovitz, 1977, 1978), the mackerel Scomberomorus
cavalla (Morgan & King, 1983), the scabbard fish Trichiurus lepturus (Morgan, 1977), the surgeonfish Prionurus microlepidotus (Wakita, Itoh & Kobayashi,
1977), the characiforms Rhaphiodon vulpinus (Roberts, 1967) and Ctenolucius hujeta (Lawson & Manly,
1973), cichlids (e.g. Huysseune, Ruber & Verheyen,
1999), and some zoarcids (Gosztonyi, 1984). Haphazard or irregular patterns of replacement were documented for some characiforms (Roberts, 1967), the cod
Gallus callarias (Holmbakken & Fosse, 1973), the
smelt Hypomesus transpacificus (Komada, 1983), two
species of gobies (Mochizuki & Fukui, 1983; Mochizuki, Fukui & Gultneh, 1991), and some zoarcids (Gosztonyi, 1984), as well as the nonteleost bowfin, Amia
calva (Miller & Radnor, 1970).
FORMATION OF MULTICUSPID TEETH IN CHARACIFORMS
The idea that multicuspid teeth in characiforms represent compound elements formed by the fusion of
conical teeth has been in the literature for a long time
(e.g. Roberts, 1967; Brewster, 1986). Fused or ‘coalesced’ teeth are known from other teleost (Andreucci,
Britski & Carneiro, 1982; Britski et al., 1985; Streelman et al., 2002) and nonteleost (Huysseune & Sire,
1998) fish groups. Fused oral teeth in scarids are also
an adult specialization; very young scarids possess
separate teeth (Chen, 2002). However, these fused
teeth are structurally different from characiform
teeth. We have shown that, at least in A. mexicanus,
multicuspid teeth are not compound elements, and
appear to share more similarities in structure and
development with mammalian molars than with
‘coalesced’ teeth in other teleosts. In cleared-andstained fish, partially mineralized multicuspid tooth
germs may appear to be composed of separate conical
elements, but this is an artefact of Alizarin staining
combined with mineralization pattern.
TRANSITION
TO ADULT DENTITION
Owing to the conserved nature of first-generation
dentitions, teleost dental specializations must arise
through subsequent tooth generations. In many cases,
changes in dental morphology correspond with ontogenetic shifts in trophic behaviour. While no studies
have investigated ontogenetic dietary changes in
A. mexicanus, such changes have been documented in
other characids (e.g. Hahn et al., 2000), including
Astyanax species (Esteves, 1996). We have shown that
in the oral dentition of A. mexicanus, unicuspid teeth
are replaced by bi- or tricuspid teeth and subsequently
by teeth with more cusps. This matches recent observations on another characiform, Alestes stuhlmannii
(Murray, 2004). In both species, widely spaced conical
teeth on the jaws of younger fish are replaced by
tightly packed multicuspid teeth in adults. Young fish
have one row of premaxillary teeth whereas older fish
have two; total number of teeth, however, remains
approximately constant and the possibility exists that
the same tooth families produce both juvenile and
adult premaxillary dentitions, simply sorting from one
to two rows.
In some teleosts, teeth may remain similar in shape
throughout life, or may be lost in adults. However,
when tooth form does change, a trend of increasing
dental complexity through successive tooth generations is most often observed (Roberts, 1967). One
exception may be the characiform genus Hydrocynus
(tigerfish), in which tricuspid jaw teeth are succeeded
by unicuspid teeth in adults; however, even in this
case, the tricuspid teeth are preceded by a conical
juvenile dentition (Brewster, 1986).
Changes in the oral dentition of A. mexicanus do not
occur uniformly. Tooth families on the premaxillae and
on the rostral portion of the lower jaws undergo drastic changes during the first few tooth generations,
whereas those located caudally on the lower jaws are
less affected and may remain small and conical, even
in large adults. These caudal teeth do not show the
changes in location of replacement teeth, replacement
pattern, or size present in more rostral multicuspid
teeth.
Those teeth that undergo this transition also
undergo three additional changes: a switch from
extraosseous to intraosseous development of replacement teeth, from haphazard to simultaneous
tooth replacement, and an exceptionally large size
increase.
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145, 523–538
A. MEXICANUS ORAL DENTITION
WHY
DO THESE CHANGES OCCUR IN COORDINATED
FASHION?
Had we shown that multicuspid teeth in this species
were coalescent elements, the observed size increase
could be due to this coalescence. Coalescence might be
due to crowding of individual conical elements in an
intraosseous location. Instead, we have rejected the
hypothesis of coalescence and the reverse appears to
be true: we speculate that selection for larger, multicuspid teeth necessitated the other changes as byproducts. There simply is not enough room in the soft
epithelial tissue for large multicuspid teeth to form
without interfering with food acquisition, and so these
teeth must develop in an out-of-the-way location,
either within or behind the bone.
Unlike the teeth of piranhas, those of A. mexicanus
do not interlock, and there is no a priori reason to suppose that they would be replaced simultaneously.
However, extensive resorption and presumably weakening of the bone are associated with intraosseous
tooth replacement in this species; were this occurring
continuously in alternate or haphazard tooth positions, it would likely be highly disruptive to the food
acquisition process. Simultaneous replacement minimizes this disruption, especially when jaw quadrants
are out of phase with one another, as we observed. It is
likely that the bone is weak during replacement, and
we predict a reduction or cessation of feeding activity
at this time.
A further question involves the relationship between
the size of teeth, their form and the location where
they develop. We believe that this relationship in
A. mexicanus is reflective of function rather than any
developmental constraint. Evidence for this assertion
comes from our occasional observations of small multicuspid teeth in the caudal region of the lower jaws in
A. mexicanus. Observations in other characiform taxa
also support this hypothesis. Taxa within the genus
Bramocharax possess oral dentitions generally similar
to those in Astyanax; however, Rosen (1972) figured
large unicuspid teeth in the rostral region and small
multicuspid (and intermixed multicuspid and unicuspid) teeth in the caudal region of one taxon
(B. bransfordi bransfordi). More broadly, he pointed
out the independence of tooth size and tooth form in
this genus (Rosen, 1972); therefore, large teeth need
not be multicuspid and small teeth need not unicuspid.
As far as we are aware, there are no other data on
the scaling of successive sets of oral teeth in teleosts.
Our results indicate about a two-fold increase in tooth
height between tooth generations, with the exception
of the transition from unicuspid to tricuspid teeth,
where tooth height increased by five times. As noted
above, we believe these scaling relationships in
A. mexicanus may be important for food acquisition
535
and/or reflect constraints imposed by jaw growth, but
likely do not reflect developmental constraints on the
teeth themselves. However, at some level, developmental constraints must become important. In particular, there must be a minimum feasible size of a
multicuspid tooth (both in teleosts and in mammals;
see Bloch, Rose & Gingerich, 1998), and this should be
larger than the minimum unicuspid tooth size. What
that minimum size is, and whether the first multicuspid teeth to appear during ontogeny in a teleost like
A. mexicanus approach it, are subjects for further
study.
ACKNOWLEDGEMENTS
We would like to thank William R. Jeffery at the University of Maryland for providing the fish from which
those used in this study were derived. We would also
like to thank Ned Friedman at the University of Colorado for allowing us use of his microscopy and imaging set-up, William Jackman, Jason Pardo and Sarah
Wise for discussion and input on the ideas expressed
in this paper, and an anonymous reviewer for their
helpful critique of the manuscript. This research was
supported by National Science Foundation Grant IBN0092487 to DWS.
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