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An asymmetric dental formula in a mammal, the São Tome Island fruit bat
Myonycteris brachycephala (Mammalia: Megachiroptera)
JAVIER JUSTE AND CARLOS IBAFEZ
Estación BiolOgica de Donana (CSIC), Sevilla 41080, Spain
JUSTE, J., and IBANEZ, C. 1993. An asymmetric dental formula in a mammal, the São Tome Island fruit bat Myonycteris
brachycephala (Mammalia: Megachiroptera)..
The dental formula in heterodont mammals characteristically shows bilateral symmetry. Its expression is likely to be subject
to very strong selective pressures, since it is associated with such basic functions as the acquisition and preparation of food.
Here we report the exceptional finding of the first asymmetric dental formula in a heterodont mammal observed in the São
Tome Island (West Africa) frugivorous bat Myonycteris brachycephala. The asymmetry results from the absence of a lower
internal incisor, occurring variably in the right or left mandible. This morphological innovation is possibly related to a
developmental instability associated with the colonization by the island species.
JUSTE, J., et IBAEz, C. 1993. An asymmetric dental formula in a mammal, the S1.o. Tonid Island fruit bat Myonycteris
brachycephala (Mammalia: Megachiroptera).
La formule dentaire des mammifères hétérodontes est normalement caractérisée par la symétrie bilatérale. Son expression
est en général le reflet de pressions de selection trés fortes parce qu’elle est associée a des fonctions aussi fondamentales
que l’acquisition et Ia preparation de Ia nourriture. La formule dentaire asymétrique que nous décrivons ici, la premièrejamais
rencontrée chez un mammifère hétérodonte, le chauve-souris frugivore Myonycteris brachycephala de l’ile São Tome
(Afrique de l’Ouest), reflète donc un phénomène tout a fait exceptionnel. Cette asymétrie résulte de l’absence d’une incisive
inférieure interne, soit a gauche, soit a droite. Cette nouveauté morphologique est peut-être reliée a l’instabiité évolutive
associée au processus de colonisation de cette espèce dans l’ile.
[Traduit par la redaction]
2
Fin. 1. Detail in upper (above) and frontal (below) view of lower incisors of Myonycteris brachycephala. A unique inner incisor is always
set in a central position, located variably in the left (A and B) or the right (C and D) mandible.
Bilateral asymmetry in structural pattern is a primary feature of nonsessile animals (Romer and Parsons 1986; Gould
1989). Although there are examples of different types of
asymmetry in living organisms (Neville 1976), there is no
record of an asymmetric dental formula in either extant or
fossil mammals. A partial exception is the narwhal (Monodon
monoceros), which has only two permanent teeth in the upper
jaw, one of which (normally the left) develops disproportionately in most males (Walker et a!. 1968). Symmetric dental
formulae are therefore evolutionarily strongly fixed, being one
of the most constant morphological characters of heterodont
mammals and a feature commonly used for evolutionary and
taxonomic studies.
The São Tome fruit bat (Myonycteris brachycephala) is
endemic to São Tome Island in the Gulf of Guinea (West
Africa). The holotype, captured in 1868 and described by
Bocage (1889), was the sole specimen known until it disappeared in a fire. In a revision of the suborder Megachiroptera, Anderson (1912) studied this holotype and recognized so
many noticeable cranial and dental differences with respect to
Myonycteris torquata, the closest continental species widespread throughout the rain forest block, that he placed
M. brachycephala in its own subgenus, Phylletis. A new species, Myonycteris relicta, recently described from a small area
in the eastern forest block (Bergmans 1980), completes this
African genus.
In the above-mentioned revision, Anderson referred in a
footnote to the presence of three lower incisors. He pointed
out that the single middle lower incisor completely filled the
space between the two external ones but considered this an
individual dental anomaly, since two pairs are characteristic of
the genus. It was only in the last decade that a second specimen
was obtained (Feiler 1984). During 1988 and 1989, we collected 19 new bats (8 males and 11 females) of this species
from the islands of the Gulf of Guinea for a revision of the
Chiroptera. The series shows a permanent dentition, all the
specimens being adults, except for three subadults, according
to cranial-suture and phalanx-ossification age criteria (Anthony
1988).
The external lower incisors (12) in the new specimens are
similar in size and shape. In all cases there is a single central
incisor, clearly smaller, with a crown diameter no more than
3/4 of the diameter of the external ones (Fig. 1). This produces
an asymmetric and exceptional dental formula. Because the
mandibular symphysis is completely fused in all the specimens, at first sight it is not possible to identify the mandible
to which it belongs. However, the ‘2 teeth of M. brachycephala have an asymmetric shape, with a more developed
223
NOTES
anterior lobe that corresponds to the anterior cuspid of the
same teeth in the closely related species M. torquata (Bergmans 1976). The odd incisor also presents one more developed
lobe with a concavity lateral to it. The lobe is visible in the
mid-incisor in 18 out of the 19 specimens. This fact, together
with the asymmetry in the arrangement of the anterior mental
foramina, as well as the distance from the 12 teeth to the
respective canines and the differential wear of the central incisor crown cuspid in some individuals, shows that either the left
(n = 13) or the right incisor (n = 6) may remain (statistically
nonsignificant difference, x2 = 2.58, p = 0.108). Moreover,
there is no evidence of a scar in any individual, including the
younger ones, or any trace of a fourth alveolus.
Asymmetries involving dental anomalies include unilateral
hyperdontia and anodontia described for several mammals but
always as rare individual characters (e.g., Van Valen 1964;
Paulinov 1975; Wolsan 1984a, 1984b). In bats specifically,
among African species these anomalies are more frequent in
phytophagous species than in animalivorous ones (Eisentraut
1956) and have been also documented for American bats
(Phillips and Jones 1969; Phillips 1971; Ramfrez Pulido and
Mudespacher 1987). In neotropical frugivorous bats (subfamily Stenodermatinae), unilateral lower-incisor agenesis can
reach 0.43% (n = 693) (Ramfrez Pulido and MUdespacher
1987), a probable overestimate since it may include some
early loss of teeth.
Such loss of a lower incisor has not been reported in the
genus Myonycteris in the approximately 200 revised specimens of either M. torquata or M. relicta (Bergmans 1976,
1980; Schlitter and McLaren 1981), nor in the 55 specimens
of M. torquaca in our own collection. Nevertheless, the
anomaly in M. brachycephala could have been carried to the
island by the first colonizing bats and could have become fixed
in the population by a nondirectional mechanism. It seems
more plausible to assume that the morphological asymmetry
was part of the expression of either a structural gene mutation
or a reordering of the initial genetic material (Muller and
Wagner 1991), in line with the disequilibrium associated with
a reduced founder population size (Mayr 1954; Levin 1970;
Carson and Templeton 1984). This mechanism has been used
to explain both dental and other anomalies in certain isolated
populations (Van Vuren and Coblentz 1988; Bouwmeester
et al. 1989; Sarre and Dearn 1991). Hence, genomic modifications capable of destabilizing dental development trends or of
changing their epigenetic interactions (Waddington 1957;
Oster and Alberch 1982) can stochastically inhibit the growth
of either inner incisor. An alternative interpretation would be
the existence of a median primordium which would come variably under the influence of right or left positional information;
nevertheless, it seems less likely, since two different bones are
involved. According to Van Valen’s (1962) classification of
asymmetries, this would be a clear example of antisymmetry.
Lower incisors apparently show scant functionality in bats
(Slaughter 1970), therefore the asymmetry would be almost
neutral. With the displacement of the remaining incisor toward
the mandibular symphysis, both the plasticity and regulation
of the implied systems (Muller 1990) would have permitted
the asymmetry to persist. The small size of São Tome Island
(836 km2), its oceanic character, and its relatively long distance from the continent (280 km) would have ensured the
maintenance of the asymmetry by hindering genetic flow in an
ecologically free environment. In fact, in contrast to the more
than 10 species of a fruit bat guild in a West African continental community (Eisentraut 1963), São Tome Island is home to
only three fruit bats (Feiler 1984). Unlike other conspicuous
asymmetries (Neville 1976; Benkman and Lindholm 1991),
this case illustrates the fixation of a nonadaptive asymmetry in
nature.
Acknowledgements
We thank Eduardo Costas, Victoria Lopez Rodas, Pere
Alberch, Miguel Delibes, Javier Castroviejo, and the Doñana
staff for their stimulating discussions; J. E. Fa and J. Palmeirim
for review of the manuscript, and L. Van Valen and an anonymous reviewer for helpful comments. The photographs were
kindly made in the Museo de Ciencias Naturales, Madrid.
This work was supported by the Spanish Instituto de Cooperacidn para el Desarrollo.
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