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The glomerular array in the olfactory bulb of many vertebrates is segregated into molecularly and anatomically distinct clusters linked to different olfactory functions. In anurans, glomerular clustering is so far only described in Xenopus laevis. We traced olfactory projections to the bulb in tadpoles belonging to six distantly related anuran species in four families (Pipidae, Hylidae, Bufonidae, Dendrobatidae) and found that glomerular clustering is remarkably conserved. The general bauplan consists of four unequally sized glomerular clusters with minor inter-species variation. During metamorphosis, the olfactory system undergoes extensive remodeling. Tracings in metamorphotic and juvenile Dendrobates tinctorius and Xenopus tropicalis suggest a higher degree of variation in the glomerular organization after metamorphosis is complete. Our study highlights, that the anatomical organization of glomeruli in the main olfactory bulb (MOB) is highly conserved, despite an extensive ecomorphological diversification among anuran tadpoles, which suggests underlying developmental constraints.
Figure 1. Diversity of anuran tadpoles used in this study. (A) The phylogenetic tree on the left is pruned from Pyron (2014), which originally includes 3,309 species. The four families to which the six examined species belong are highlighted. The middle panel describes the six species based on phylogeny, ecology, and morphology. Both Xenopus species belong to earlier diverging mesobatrachians, lack keratinized mouthparts (morphotype I), and are thus obligate suspension feeders. The four neobatrachian species can all be classified as morphotype IV. Their developed mouthparts enable them to scrape off food from the substrate. The two dendrobatid species both receive parental care and mostly live in pools in leaf axils or bromeliads. Morphotype distinction follows (Orton, 1953) and ecomorphotypic categorizations are based on (Altig and Johnston, 1989). (B) Experimental concept of this study. We tried to examine whether the glomerular organization in the main olfactory bulb (MOB) of tadpoles is influenced by the respective habitat or feeding mechanisms in the distantly related species.
Figure 2. Glomerular clustering in the MOB is conserved among anuran tadpoles. (A) Glomeruli in the MOB of all species can be segregated into three ventrally (LC, IC, MC) and one dorso-medially located clusters (DC). White dotted lines—cluster outlines, filled arrowheads—glomeruli, empty arrowhead—small glomerular cluster, asterisks—ventral and dorsal lobes of the LC. (B) The relative volume of the clusters (schematically shown on the left) varies between the four families. The volumes of the clusters relative to the total glomerular volume for each family are shown. Each dot represents one MOB hemisphere and species of the same family are grouped. Significance levels: ***p < 0.001, **p < 0.01, *p < 0.05. A, anterior; P, posterior; L, lateral; M, medial; D, dorsal; V, ventral; ON, olfactory nerve; MOB, main olfactory bulb; LC, lateral cluster; IC, intermediate cluster; MC, medial cluster; DC, dorsomedial cluster; PI, Pipidae; HY, Hylidae; BU, Bufonidae; DB, Dendrobatidae.
Figure 3. Metamorphotic changes of glomerular clusters in Xenopus tropicalis and Dendrobates tinctorius. Before metamorphosis (top), the left and right glomerular projections in the MOB are separated at the midline (vertical line). During metamorphosis, the dorsomedial components form an unpaired dorsal cluster (middle). In the late phases of metamorphosis (bottom), the ventral glomerular clusters in X. tropicalis are unchanged, while they are reduced in D. tinctorius (asterisks). Arrowheads—extrabulbar fibers. The numbers next to the images indicate the developmental stages after Nieuwkoop and Faber for X. tropicalis and Gosner for D.tinctorius. A, anterior; P, posterior; D, dorsal; V, ventral; ON, olfactory nerve; MOB, main olfactory bulb.
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