RESUMO
The aquatic-to-terrestrial shift in the life cycle of most anurans suggests that the differences between the larval and adult morphology of the nose are required for sensory function in two media with different physical characteristics. However, a better controlled test of specialization to medium is to compare adult stages of terrestrial frogs with those that remain fully aquatic as adults. The Ceratophryidae is a monophyletic group of neotropical frogs whose diversification from a common terrestrial ancestor gave rise to both terrestrial (Ceratophrys, Chacophrys) and aquatic (Lepidobatrachus) adults. So, ceratophryids represent an excellent model to analyze the morphology and possible changes related to a secondary aquatic life. We describe the histomorphology of the nose during the ontogeny of the Ceratophryidae, paying particular attention to the condition in adult stages of the recessus olfactorius (a small area of olfactory epithelium that appears to be used for aquatic olfaction) and the eminentia olfactoria (a raised ridge on the floor of the principal cavity correlated with terrestrial olfaction). The species examined (Ceratophrys cranwelli, Chacophrys pierottii, Lepidobatrachus laevis, and L. llanensis) share a common larval olfactory organ composed by the principal cavity, the vomeronasal organ and the lateral appendix. At postmetamorphic stages, ceratophryids present a common morphology of the nose with the principal, middle, and inferior cavities with characteristics similar to other neobatrachians at the end of metamorphosis. However, in advanced adult stages, Lepidobatrachus laevis presents a recessus olfactorius with a heightened (peramorphic) development and a rudimentary (paedomorphic) eminentia olfactoria. Thus, the adult nose in Lepidobatrachus laevis arises from a common developmental 'terrestrial' pathway up to postmetamorphic stages, when its ontogeny leads to a distinctive morphology related to the evolutionarily derived, secondarily aquatic life of adults of this lineage.
Assuntos
Anuros/anatomia & histologia , Anuros/crescimento & desenvolvimento , Evolução Biológica , Mucosa Olfatória/anatomia & histologia , Mucosa Olfatória/crescimento & desenvolvimento , Animais , Larva/anatomia & histologia , Larva/crescimento & desenvolvimento , Órgão Vomeronasal/anatomia & histologia , Órgão Vomeronasal/crescimento & desenvolvimentoRESUMO
The anuran peripheral olfactory system is composed of a number of subsystems, represented by distinct neuroepithelia. These include the main olfactory epithelium and vomeronasal organ (found in most tetrapods) and three specialized epithelia of anurans: the buccal-exposed olfactory epithelium of larvae, and the olfactory recess and middle chamber epithelium of postmetamorphic animals. To better characterize the developmental changes in these subsystems across the life cycle, morphometric changes of the nasal chemosensory organs during larval development and metamorphosis were analyzed in three different anuran species (Rhinella arenarum, Hypsiboas pulchellus, and Xenopus laevis). We calculated the volume of the nasal chemosensory organs by measuring the neuroepithelial area from serial histological sections at four different stages. In larvae, the vomeronasal organ was relatively reduced in R. arenarum compared with the other two species; the buccal-exposed olfactory epithelium was absent in X. laevis, and best developed in H. pulchellus. In postmetamorphic animals, the olfactory epithelium (air-sensitive organ) was relatively bigger in terrestrial species (R. arenarum and H. pulchellus), whereas the vomeronasal and the middle chamber epithelia (water-sensitive organs) was best developed in X. laevis. A small olfactory recess (likely homologous with the middle chamber epithelium) was found in R. arenarum juveniles, but not in H. pulchellus. These results support the association of the vomeronasal and middle chamber epithelia with aquatic olfaction, as seen by their enhanced development in the secondarily aquatic juveniles of X. laevis. They also support a role for the larval buccal-exposed olfactory epithelium in assessment of oral contents: it was absent in X. laevis, an obligate suspension feeder, while present in the two grazing species. These initial quantitative results give, for the first time, insight into the functional importance of the peripheral olfactory subsystems across the anuran life cycle.
Assuntos
Anuros/crescimento & desenvolvimento , Metamorfose Biológica , Mucosa Olfatória/crescimento & desenvolvimento , Órgão Vomeronasal/crescimento & desenvolvimento , Animais , Epitélio/anatomia & histologia , Processamento de Imagem Assistida por Computador , Imuno-Histoquímica , Larva/crescimento & desenvolvimento , Mucosa Olfatória/anatomia & histologia , Especificidade da Espécie , Órgão Vomeronasal/anatomia & histologia , Xenopus laevis/crescimento & desenvolvimentoRESUMO
We investigated the occurrence and anatomy of the vomeronasal system (VNS) in tadpoles of 13 different anuran species. All of the species possessed a morphologically fully developed VNS with a highly conserved anatomical organisation. We found that a bean-shaped vomeronasal organ (VNO) developed early in the tadpoles, during the final embryonic stages, and was located in the anteromedial nasal region. Histology revealed the presence of bipolar chemosensory neurones in the VNO that were immunoreactive for the Gαo protein. Tract-tracing experiments demonstrated that chemosensory neurones from the VNO reach specific areas in the brain, where a discernible accessory olfactory bulb (AOB) could be observed. The AOB was located in the ventrolateral side of the anterior telencephalon, somewhat caudal to the main olfactory bulb. Synaptophysin-like immunodetection revealed that synaptic contacts between VNO and AOB are established during early larval stages. Moreover, using lectin staining, we identified glomerular structures in the AOB in most of the species that we examined. According to our findings, a significant maturation in the VNS is achieved in anuran larvae. Recent published evidence strongly suggests that the VNS appeared early in vertebrate evolution and was already present in the aquatic last common ancestor of lungfish and tetrapods. In this context, tadpoles may be a good model in which to investigate the anatomical, biochemical and functional aspects of the VNS in an aquatic environment.
Assuntos
Anuros/anatomia & histologia , Órgão Vomeronasal/anatomia & histologia , Animais , Anuros/crescimento & desenvolvimento , Imuno-Histoquímica , Larva/anatomia & histologia , Bulbo Olfatório/anatomia & histologia , Especificidade da Espécie , Órgão Vomeronasal/crescimento & desenvolvimentoRESUMO
The vomeronasal organ (VNO) is a tubular chemoreceptory organ which detects environmental pheromones and is essential for mammalian normal reproductive activity. A sensitive chemoreceptory neuroepithelium lines the concave VNO wall and the opposite, convex wall is lined by a seudostratified, receptor-free epithelium. The secretion of the Jacobson glands (JG) -tubuloacinary glands lying in the lamina propia of the VNO - is essential for pheromones contacting vomeronasal organ chemoreceptors. Tubuloacinary glands lying in the connective tissue of the nasal septum mucosa (Bowman glands), can be classified as ventral and dorsal, according to their location. Positivity to PAS and Alcyan blue reactions and androgen receptor immunolocalization was evaluated with a semiquantitative system (0,1, 2 or 3 crosses) in JG, ventral Bowman glands (VBG), dorsal Bowman glands (DBG), sensitive chemoreceptory neuroepithelium (Ne), receptor-free epithelium (RFE) and nasal septum respiratory epithelium (RE) histological slides of male rats at 5, 15, 25 and 35 days of age. The VBG and JG were intensely positive to PAS reaction since 5 days of age, and weakly positive to Alcyan blue reaction (AB) since 15 days of age, but not at 5 days of age. Both JG and VBG were strongly positive to androgen receptor immunolocalization at all ages studied (15, 25 and 35 days of age). DBG were always negative to both PAS and AB reactions. The NE and the RFE and nasal mucosa luminar epithelium were negative. To our knowledge, this is the first report of androgen receptor (AR) immunolocalization in the vomeronasal organ and the nasal septum mucosa. The present results also suggest an influence of androgens on the mechanism of pheromones contacting with the Ne of the VNO through regulation of the Jacobson glands secretion.
El órgano vomeronasal (VNO) es un órgano quimioreceptor, tubular, que detecta feromonas ambientales. Es esencial para la actividad reproductiva normal de los mamíferos. El VNO está formado por un neuroepitelio quimiosensible (pared cóncava, Ne) y un epitelio pseudoestratificado (epitelio libre de receptores: RFE) en la pared opuesta, convexa. La secreción de las glándulas tubuloacinares de Jacobson (JG), ubicadas en la lámina propia del VNO, son esenciales para que las feromonas entren en contacto con el Ne. Las glándulas tubuloacinares ubicadas en la mucosa del tabique nasal (glándulas del Bowman), se pueden clasificar como ventrales (VBG) y dorsales (DBG), según su localization. La positividad a las técnicas de PAS, Azul de Alcián (AB) e immunolocalization del receptor de andrógeno (AR), fueron evaluadas con un sistema semicuantitativo (0, 1, 2 o 3 cruces) en láminas histológicas de JG, VBG, DBG, Ne, RFE y del epitelio del tabique nasal (RE) en ratas macho de 5, 15, 25 y 35 días de edad. Las VBG y JG fueron intensamente positivas a la reacción de PAS desde los 5 días de edad y débilmente positivas a la reacción de AB desde los 15 días de edad, pero no a los 5 días de la edad. Las JG y VBG fueron fuertemente positivas a la immunolocalization del AR en las edades estudiadas (15, 25 y 35 días de edad). Las DBG fueron siempre negativas a las reacciones de PAS y AB. El NE, el RFE y el RE fueron negativos. Según nuestro conocimiento, éste es el primer informe de immunolocalization del AR en el VNO y la mucosa del tabique nasal. Los actuales resultados sugieren una influencia de los andrógenos en el mecanismo por el cual entran en contacto las feromonas y el Ne, a través de la regulación por andrógenos de la secreción de las JG.