Click here to close
Hello! We notice that you are using Internet Explorer, which is not supported by Xenbase and may cause the site to display incorrectly.
We suggest using a current version of Chrome,
FireFox, or Safari.
???displayArticle.abstract???
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.
Baier,
Olfactory glomeruli in the zebrafish form an invariant pattern and are identifiable across animals.
1994, Pubmed
Baier,
Olfactory glomeruli in the zebrafish form an invariant pattern and are identifiable across animals.
1994,
Pubmed Bear,
The Evolving Neural and Genetic Architecture of Vertebrate Olfaction.
2016,
Pubmed Benzekri,
Olfactory metamorphosis in the coastal tailed frog Ascaphus truei (Amphibia, Anura, Leiopelmatidae).
2012,
Pubmed BLOOM,
Studies on the olfactory epithelium of the frog and the toad with the aid of light and electron microscopy.
1954,
Pubmed Braubach,
Distribution and functional organization of glomeruli in the olfactory bulbs of zebrafish (Danio rerio).
2012,
Pubmed Brinkmann,
One Special Glomerulus in the Olfactory Bulb of Xenopus laevis Tadpoles Integrates a Broad Range of Amino Acids and Mechanical Stimuli.
2016,
Pubmed
,
Xenbase Brown,
Divergence in parental care, habitat selection and larval life history between two species of Peruvian poison frogs: an experimental analysis.
2008,
Pubmed Buck,
A novel multigene family may encode odorant receptors: a molecular basis for odor recognition.
1991,
Pubmed Date-Ito,
Xenopus V1R vomeronasal receptor family is expressed in the main olfactory system.
2008,
Pubmed
,
Xenbase Dulac,
A novel family of genes encoding putative pheromone receptors in mammals.
1995,
Pubmed Eisthen,
Evolution of vertebrate olfactory systems.
1997,
Pubmed Fischer,
Neural correlates of winning and losing fights in poison frog tadpoles.
2020,
Pubmed Frontini,
Glomerular territories in the olfactory bulb from the larval stage of the sea lamprey Petromyzon marinus.
2003,
Pubmed Gaudin,
3D atlas describing the ontogenic evolution of the primary olfactory projections in the olfactory bulb of Xenopus laevis.
2005,
Pubmed
,
Xenbase Gliem,
Bimodal processing of olfactory information in an amphibian nose: odor responses segregate into a medial and a lateral stream.
2013,
Pubmed
,
Xenbase Green,
Odorant organization in the olfactory bulb of the sea lamprey.
2017,
Pubmed Greer,
A Family of non-GPCR Chemosensors Defines an Alternative Logic for Mammalian Olfaction.
2016,
Pubmed Hamdani,
Is feeding behaviour in crucian carp mediated by the lateral olfactory tract?
2001,
Pubmed Hamdani,
The functional organization of the fish olfactory system.
2007,
Pubmed Hansen,
Differential distribution of olfactory receptor neurons in goldfish: structural and molecular correlates.
2004,
Pubmed Hansen,
Ultrastructure of the olfactory organ in the clawed frog, Xenopus laevis, during larval development and metamorphosis.
1998,
Pubmed
,
Xenbase Hansen,
Correlation between olfactory receptor cell type and function in the channel catfish.
2003,
Pubmed Hassenklöver,
Olfactory wiring logic in amphibians challenges the basic assumptions of the unbranched axon concept.
2013,
Pubmed
,
Xenbase Herrada,
A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution.
1997,
Pubmed Jermakowicz,
Development of the nasal chemosensory organs in two terrestrial anurans: the directly developing frog, Eleutherodactylus coqui (Anura: Leptodactylidae), and the metamorphosing toad, Bufo americanus (Anura: Bufonidae).
2004,
Pubmed Jungblut,
Heterogeneous distribution of G protein alpha subunits in the main olfactory and vomeronasal systems of Rhinella (Bufo) arenarum tadpoles.
2009,
Pubmed
,
Xenbase Jungblut,
Quantitative comparative analysis of the nasal chemosensory organs of anurans during larval development and metamorphosis highlights the relative importance of chemosensory subsystems in the group.
2017,
Pubmed
,
Xenbase Liberles,
A second class of chemosensory receptors in the olfactory epithelium.
2006,
Pubmed Manzini,
cAMP-independent olfactory transduction of amino acids in Xenopus laevis tadpoles.
2003,
Pubmed
,
Xenbase Manzini,
Presynaptic protein distribution and odour mapping in glomeruli of the olfactory bulb of Xenopus laevis tadpoles.
2007,
Pubmed
,
Xenbase Manzini,
cAMP-independent responses of olfactory neurons in Xenopus laevis tadpoles and their projection onto olfactory bulb neurons.
2002,
Pubmed
,
Xenbase Menini,
Olfactory Coding in Larvae of the African Clawed Frog Xenopus laevis
2010,
Pubmed Munger,
Subsystem organization of the mammalian sense of smell.
2009,
Pubmed Nezlin,
Organization of glomeruli in the main olfactory bulb of Xenopus laevis tadpoles.
2003,
Pubmed
,
Xenbase Preibisch,
Globally optimal stitching of tiled 3D microscopic image acquisitions.
2009,
Pubmed Pyron,
Biogeographic analysis reveals ancient continental vicariance and recent oceanic dispersal in amphibians.
2014,
Pubmed Reiss,
Metamorphic remodeling of the primary olfactory projection in Xenopus: developmental independence of projections from olfactory neuron subclasses.
1997,
Pubmed
,
Xenbase Rivière,
Formyl peptide receptor-like proteins are a novel family of vomeronasal chemosensors.
2009,
Pubmed Roelants,
Anuran radiations and the evolution of tadpole morphospace.
2011,
Pubmed Sato,
Mutually exclusive glomerular innervation by two distinct types of olfactory sensory neurons revealed in transgenic zebrafish.
2005,
Pubmed Schindelin,
Fiji: an open-source platform for biological-image analysis.
2012,
Pubmed Syed,
Coordinated shift of olfactory amino acid responses and V2R expression to an amphibian water nose during metamorphosis.
2017,
Pubmed
,
Xenbase Syed,
Ancestral amphibian v2rs are expressed in the main olfactory epithelium.
2013,
Pubmed
,
Xenbase Terni,
Functional Evaluation of Olfactory Pathways in Living Xenopus Tadpoles.
2018,
Pubmed
,
Xenbase Veeranagoudar,
Foraging behaviour in tadpoles of the bronze frog Rana temporalis: experimental evidence for the ideal free distribution.
2004,
Pubmed Weiss,
Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibians.
2020,
Pubmed
,
Xenbase
