Evolution of the structure and function of the vertebrate tongue

Abstract

Studies of the comparative morphology of the tongues of living vertebrates have revealed how variations in the morphology and function of the organ might be related to evolutional events. The tongue, which plays a very important role in food intake by vertebrates, exhibits significant morphological variations that appear to represent adaptation to the current environmental conditions of each respective habitat. This review examines the fundamental importance of morphology in the evolution of the vertebrate tongue, focusing on the origin of the tongue and on the relationship between morphology and environmental conditions. Tongues of various extant vertebrates, including those of amphibians, reptiles, birds and mammals, were analysed in terms of gross anatomy and microanatomy by light microscopy and by scanning and transmission electron microscopy. Comparisons of tongue morphology revealed a relationship between changes in the appearance of the tongue and changes in habitat, from a freshwater environment to a terrestrial environment, as well as a relationship between the extent of keratinization of the lingual epithelium and the transition from a moist or wet environment to a dry environment. The lingual epithelium of amphibians is devoid of keratinization while that of reptilians is keratinized to different extents. Reptiles live in a variety of habitats, from seawater to regions of high temperature and very high or very low humidity. Keratinization of the lingual epithelium is considered to have been acquired concomitantly with the evolution of amniotes. The variations in the extent of keratinization of the lingual epithelium, which is observed between various amniotes, appear to be secondary, reflecting the environmental conditions of different species.

Figure 1

Surface structure and histology of the dorsal epithelium of the tongues of amphibians. (a-c) Genus Rana. (a) Scanning electron micrograph of the tongue of Rana catesbeiana. (b) Light micrograph of a filiform papilla of Rana rugosa rugosa. (c) High-magnification transmission electron micrograph of the filiform papillae of Rana rugosa rugosa. (d-g) Genus Bufo (Bufo japonicus). (d) Scanning electron micrograph. (e) Light micrograph. (f,g) Transmission electron micrographs. Both Rana and Bufo have sensory discs that contain taste buds (arrows in a,d) and are scattered between filiform papillae (arrowheads in a) or ridge-like papillae (arrowheads in d). In Rana and Bufo, most cells of the lingual epithelium contain secretory granules (arrows in b,c,e,f). However, the cells at the tips of the filiform or ridge-like papillae are significantly different in Rana (b,c) and Bufo (e-g). Arrowheads in (e) show such cells in Bufo; they contain no secretory granules. (g) A high-magnification view of the cells in (e). Scale bars = 300 μm (a); 20μm (b); 1 μm (c); 100 μm (d); 50 μm (e); 2 μm (f); 5μm (g). (a, reproduced from Iwasaki & Sakata, 1985; with permission from Okajimas Folia Anatomica Japonica; b, reproduced from Iwasaki et al., 1997b; with permission from Tissue and Cell; d, reproduced from Iwasaki & Kobayashi, 1988; with permission from Zoological Science; e, reproduced from Iwasaki et al., 1989b; with permission from Zoological Science.)

Figure 2

Surface structure and histology of the epithelium of the tongues of squamate reptiles. (a-c) Scanning electron micrographs of the dorsal surface of the tongue of the Japanese lizard Takydromus tachydromoides. (a) Anterior bifurcated area. (b) Lingual body. (c) Lingual radix. Arrows in c show the secretory fluid. (d-f) Transmission electron micrographs of the dorsal epithelium of the tongues of two lizards. (d) Anterior bifurcated area of the tongue of Takydromus tachydromoides corresponding to a. (e) Lingual body of Takydromus tachydromoides corresponding to b. (f) Lingual radix of Gekko japonicus corresponding to the same region as c in Takydromus tachydromoides. Arrows show bipartite secretory granules with a dense central core. (g-i) The rat snake Elaphe climacophora. (g) Scanning electron micrograph of one of the anterior bifurcated parts of the tongue. Arrows indicate microfacets. (h) Transmission electron micrograph of the outerward face of the a-layer of the epithelium of the anterior bifurcated parts of the tongue. Arrows indicate microfacets. ( j) Light micrograph of the dorsal lingual epithelium showing a frontal section of the lingual apex at the shedding phase. Arrows indicate positive staining with Sudan III. Scale bars = 30 μm (a); 50 μm (b); 5 μm (c,g); 0.5 μm (d); 2 μm (e,f); 1 μm (h); 10 μm (i). (a-c, reproduced from Iwasaki & Miyata, 1985; with permission from Okajimas Folia Anatomica Japonica; g, reproduced from Iwasaki et al., 1996e; with permission from the Anatomical Record.)

Figure 3

Surface structure and histology of the dorsal epithelium of the tongues of turtles. (a-c) The soft-shell turtle Trionyx cartilagineus, which lives in or near freshwater. (a) Scanning electron micrograph of the surface of a low, disc-like papilla located on the dorsal side of the posterior part of the tongue. (b) Light micrograph of cells in the dorsal epithelium of the tongue. No keratinization is evident in any of the lingual epithelium. (c) Transmission electron micrograph of cells in the dorsal epithelium of the tongue. (d-f) A juvenile sea turtle, the Hawksbill turtle (Eretmochelys imbricata bissa). (d) Scanning electron micrograph. Arrows show the marginal cell border. (e) Light micrograph. Arrow indicates the keratinized, squamous, stratified epithelium.(f) Transmission electron micrograph of the keratinized layer of the epithelium. Scale bars = 100 μm (a); 30 μm (b); 2 μm (c); 3 μm (d); 10 μm (e); 0.5 μm (f). (a,c, reproduced from Iwasaki et al., 1996b; with permission from the Anatomical Record; d-f, reproduced from Iwasaki et al., 1996a; with permission from the Anatomical Record.)

Figure 4

Surface structure and histology of the dorsal epithelium of the tongue of Middendorff's bean goose, Anser fabalis middendorffii. (a) Macroscopic dorsal view of the tongue. Arrows show lingual hairs on the lateral sides). (b) Scanning electron micrograph of the lateral side of the tongue. Lingual papillae (arrows) are compactly distributed on the tongue, and large cylindrical papillae (arrowhead) are scattered among them. (c) Transmission electron micrograph of cells on the extreme surface side of the keratinized layer of the dorsal epithelium. Keratin filaments are looser than those of cells beneath this area. The surface of the cell membrane has microridges. No other organelles are visible. (d) Higher-magnification transmission electron micrograph of the cytoplasm of a cell in the keratinized layer of the epithelium of a strongly keratinized papilla. Scale bars = 10 μm (a); 500 μm (b); 2 μm (c); 0.2 μm (d). (a-c, reproduced from Iwasaki et al., 1997a; with permission from the Anatomical Record.)

Figure 5

Surface structure of the dorsal epithelium of the tongues of rats and mice during development, as demonstrated by scanning electron microscopy. (a) Rat fetus on embryonic day 12. Arrows show the rudiments of fungiform papillae. Arrowhead indicates the median sulcus. (b) Mouse fetus on embryonic day 15. Arrows indicate original rudiments of fungiform papillae. (c) Juvenile rat just after birth. Arrow indicates a fungiform papilla. Arrowheads indicate rudiments of filiform papillae. (d) Juvenile mouse 7 days after birth. Arrows indicate fungiform papillae. Arrowheads indicate filiform papillae. Scale bars = 100 μm (a); 20 μm (b, c); 50 μm (d). (a,c, reproduced from Iwasaki et al., 1997b; with permission from the Anatomical Record; b, reproduced from Iwasaki et al., 1996f; with permission from Acta Anatomica.)

Figure 6

Surface structure and histology of the epithelium of mammalian tongues. (a-c) Scanning electron micrographs of the dorsal surface of the tongue of the mongoose Herpestes edwardsi. (a) Apex of the dorsal surface. Each filiform papilla has a large bulge (arrowhead) in the baso-frontal area. About 10 small processes surround the bulge in a semicircle on the posterior side. Among these processes, the middle rear one (arrow) is the largest. (b) Anterior part of the dorsal surface. Each papilla consists of a large process without a baso-frontal bulge. (c) Middle dorsal surface. Filiform papillae (arrow) are cylindrical without a baso-frontal bulge. Interpapillar epithelium (arrowheads) appears between these papillae as a series of large protuberances with many folds on their surfaces. (d-e) Transmission electron micrographs of the dorsal epithelium of the tongue of the mongoose Herpestes edwardsi. (d) Superficial intermediate layer of the papillary epithelium. Large, droplet-like keratohyalin granules arrow) and tonofibrils (arrowhead) are recognizable. (e) Keratinized surface layer of the papillary epithelium. Keratinized and prekeratinized cells are arranged in a lamellar pattern. (f) Scanning electron micrograph of the dorsal surface of tongue of the Japanese monkey Macaca fuscata fuscata. Filiform papillae are crown-shaped, with several or more branches (arrows). g-h) Transmission electron micrographs of the dorsal epithelium of the tongue of the Japanese monkey Macaca fuscata fuscata. g) Surface layer of the anterior side of a filiform papilla. Most of the cytoplasm is occupied by filamentous structures that represent tonofilaments. (h) Deep intermediate layer of the posterior side of a filiform papilla. In most of cells, large numbers of tonofibrils are present in the cytoplasm. A large nucleus is recognizable. Scale bars = 30 μm (a); 50 μm (b); 300 μm (c); 2 μm d); 1 μm (e); 5 μm (f, g, h). (a, c, reproduced from Iwasaki et al., 1987; with permission from Acta Anatomica; d, reproduced from Iwasaki & Miyata, 1990; with permission from Journal of Anatomy.)