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. 2016 Dec;229(6):847-856.
doi: 10.1111/joa.12522. Epub 2016 Jul 22.

Complex Patterns of Tooth Replacement Revealed in the Fruit Bat (Eidolon Helvum)

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Free PMC article

Complex Patterns of Tooth Replacement Revealed in the Fruit Bat (Eidolon Helvum)

Elena M Popa et al. J Anat. .
Free PMC article

Abstract

How teeth are replaced during normal growth and development has long been an important question for comparative and developmental anatomy. Non-standard model animals have become increasingly popular in this field due to the fact that the canonical model laboratory mammal, the mouse, develops only one generation of teeth (monophyodonty), whereas the majority of mammals possess two generations of teeth (diphyodonty). Here we used the straw-coloured fruit bat (Eidolon helvum), an Old World megabat, which has two generations of teeth, in order to observe the development and replacement of tooth germs from initiation up to mineralization stages. Our morphological study uses 3D reconstruction of histological sections to uncover differing arrangements of the first and second-generation tooth germs during the process of tooth replacement. We show that both tooth germ generations develop as part of the dental lamina, with the first generation detaching from the lamina, leaving the free edge to give rise to a second generation. This separation was particularly marked at the third premolar locus, where the primary and replacement teeth become positioned side by side, unconnected by a lamina. The position of the replacement tooth, with respect to the primary tooth, varied within the mouth, with replacements forming posterior to or directly lingual to the primary tooth. Development of replacement teeth was arrested at some tooth positions and this appeared to be linked to the timing of tooth initiation and the subsequent rate of development. This study adds an additional species to the growing body of non-model species used in the study of tooth replacement, and offers a new insight into the development of the diphyodont condition.

Keywords: dental lamina; diphyodont; fruit bat; mammal; tooth development; tooth replacement.

Figures

Figure 1
Figure 1
Fruit bat embryonic development (A‐I) and adult fruit bat skull (J). (A‐I) The nine fruit bat embryos used for this study were photographed frontally in ascending order of head length. (J) Top half: bottom and top views of the adult upper and lower jaws, respectively. Bottom half: sagittal and frontal views.
Figure 2
Figure 2
Development of the fruit bat dentition from initiation to late cap stage. Frontal histological sections of upper jaw tooth germs, stained with a Picro‐Sirius Red, Alcian Blue and haematoxylin trichrome stain. (A1‐A3) First incisor. (B1‐B4) Second incisor. (C1‐C4) Canine. (D1‐D4) First premolar. (E1‐E4) Second premolar. (F1‐F4) Third premolar. (G1‐G) First molar. Asterisks mark the initiation of the second tooth generation. OC, oral cavity; OE, oral epithelium. Labial and lingual are to the left and right sides of each image, respectively. Scale bars: 100 μm.
Figure 3
Figure 3
Development of the fruit bat dentition from late cap to mineralization stage. Frontal histological sections of upper jaw tooth germs, stained with a Picro‐Sirius Red, Alcian Blue and haematoxylin trichrome stain. (A1‐A3) First incisor. (B1‐B3) Second incisor. (C1‐C3) Canine. (D1‐D3) First premolar; arrows point to enamel knot. (E1‐E3) Deciduous second premolar. DL: dental lamina (E'1‐E'3) permanent second premolar. (F1‐F3) Third premolar. (G1‐G3) First molar. OC, oral cavity; OE, oral epithelium. Labial and lingual are to the left and right sides of each image, respectively. Scale bars: 200 μm.
Figure 4
Figure 4
Interesting morphological aspects of the dental lamina. (A, A1) Frontal histological sections of lower jaw third premolar at 12.5 mm. (B, B1) Upper jaw second premolar at 16 mm; magnification of image in Fig. 3 (E3). Black arrows point to fragmenting outer enamel epithelium. Red arrows point to fragmenting dental lamina. (C, C1) Upper jaw canine at 16 mm, magnification of image in Fig. 3 (C3). Arrowheads point to dental lamina rudiment. OC, oral cavity; OE, oral epithelium. Labial and lingual are to the left and right sides of each image, respectively. All sections were stained with a Picro‐Sirius Red, Alcian Blue and haematoxylin trichrome stain. Scale bars: 50 μm.
Figure 5
Figure 5
Different modalities of tooth replacement throughout the jaw. Upper panel: three‐dimensional reconstructions of replacing tooth germs during four stages of embryonic fruit bat development. Orientation arrows: La, labial; Li, lingual; A: anterior; P, posterior; O, oral; Ab, Aboral. Ab* and F*: anterior and posterior directions are reversed for better visualisation of both tooth germs. Scale bar: 100 μm. Lower panel: Schematic diagram summarizing the different modalities of replacement tooth germ development in the fruit bat. The second‐generation tooth germ develops from the dental lamina growing on the lingual side of the first‐generation tooth germ; depending on the location in the jaw, this may develop directly on the lingual side (canine), directly posterior (second premolar) or may become completely separated from the first‐generation tooth germ (third premolar). In the case of the first premolar, no second‐generation tooth germ develops.

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