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      Conservation of Glomerular Organization in the Main Olfactory Bulb of Anuran Larvae

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          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.

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          Most cited references51

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          A novel family of genes encoding putative pheromone receptors in mammals.

          In mammals, olfactory sensory perception is mediated by two anatomically and functionally distinct sensory organs: the main olfactory epithelium (MOE) and the vomeronasal organ (VNO). Pheromones activate the VNO and elicit a characteristic array of innate reproductive and social behaviors, along with dramatic neuroendocrine responses. Differential screening of cDNA libraries constructed from single sensory neurons from the rat VNO has led to the isolation of a family of about 30 putative receptor genes. Sequence analysis indicates that these genes comprise a novel family of seven transmembrane domain proteins unrelated to the receptors expressed in the MOE. Moreover, the expression of each member of the gene family is restricted to a small subpopulation of VNO neurons. These genes are likely to encode mammalian pheromone receptors.
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            Biogeographic analysis reveals ancient continental vicariance and recent oceanic dispersal in amphibians.

            R Pyron (2014)
            Amphibia comprises over 7000 extant species distributed in almost every ecosystem on every continent except Antarctica. Most species also show high specificity for particular habitats, biomes, or climatic niches, seemingly rendering long-distance dispersal unlikely. Indeed, many lineages still seem to show the signature of their Pangaean origin, approximately 300 Ma later. To date, no study has attempted a large-scale historical-biogeographic analysis of the group to understand the distribution of extant lineages. Here, I use an updated chronogram containing 3309 species (∼ 45% of extant diversity) to reconstruct their movement between 12 global ecoregions. I find that Pangaean origin and subsequent Laurasian and Gondwanan fragmentation explain a large proportion of patterns in the distribution of extant species. However, dispersal during the Cenozoic, likely across land bridges or short distances across oceans, has also exerted a strong influence. Finally, there are at least three strongly supported instances of long-distance oceanic dispersal between former Gondwanan landmasses during the Cenozoic. Extinction from intervening areas seems to be a strong factor in shaping present-day distributions. Dispersal and extinction from and between ecoregions are apparently tied to the evolution of extraordinarily adaptive expansion-oriented phenotypes that allow lineages to easily colonize new areas and diversify, or conversely, to extremely specialized phenotypes or heavily relictual climatic niches that result in strong geographic localization and limited diversification.
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              Subsystem organization of the mammalian sense of smell.

              The mammalian olfactory system senses an almost unlimited number of chemical stimuli and initiates a process of neural recognition that influences nearly every aspect of life. This review examines the organizational principles underlying the recognition of olfactory stimuli. The olfactory system is composed of a number of distinct subsystems that can be distinguished by the location of their sensory neurons in the nasal cavity, the receptors they use to detect chemosensory stimuli, the signaling mechanisms they employ to transduce those stimuli, and their axonal projections to specific regions of the olfactory forebrain. An integrative approach that includes gene targeting methods, optical and electrophysiological recording, and behavioral analysis has helped to elucidate the functional significance of this subsystem organization for the sense of smell.
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                Author and article information

                Contributors
                Journal
                Front Neuroanat
                Front Neuroanat
                Front. Neuroanat.
                Frontiers in Neuroanatomy
                Frontiers Media S.A.
                1662-5129
                24 July 2020
                2020
                : 14
                : 44
                Affiliations
                [1] 1Department of Animal Physiology and Molecular Biomedicine, Justus-Liebig-University Giessen , Giessen, Germany
                [2] 2Departamento de Biodiversidad y Biología Experimental, IBBEA-CONICET, Universidad de Buenos Aires , Buenos Aires, Argentina
                [3] 3Department of Biology, Stanford University , Stanford, CA, United States
                Author notes

                Edited by: James C. Vickers, University of Tasmania, Australia

                Reviewed by: Ruth Morona, Complutense University of Madrid, Spain; Marissa Fabrezi, CONICET Instituto de Bio y Geociencias del NOA (IBIGEO), Argentina

                Article
                10.3389/fnana.2020.00044
                7393516
                32792916
                b57b596f-00ed-414d-b12e-8c0ed23bb4ff
                Copyright © 2020 Weiss, Jungblut, Pozzi, O’Connell, Hassenklöver and Manzini.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 11 May 2020
                : 30 June 2020
                Page count
                Figures: 3, Tables: 1, Equations: 0, References: 62, Pages: 8, Words: 6012
                Funding
                Funded by: Deutsche Forschungsgemeinschaft 10.13039/501100001659
                Funded by: National Center for Research Resources 10.13039/100000097
                Funded by: Company of Biologists 10.13039/501100000522
                Funded by: Secretaría de Ciencia y Técnica, Universidad de Buenos Aires 10.13039/501100010253
                Funded by: Consejo Nacional de Investigaciones Científicas y Técnicas 10.13039/501100002923
                Categories
                Neuroscience
                Brief Research Report

                Neurosciences
                amphibians,anura,olfaction,glomeruli,olfactory bulb,evolution
                Neurosciences
                amphibians, anura, olfaction, glomeruli, olfactory bulb, evolution

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