Ontogenetic Development of the Derived Olfactory System of the Mantellid Frog Mantidactylus betsileanus

Abstract

The nasal cavity of Mantidactylus betsileanus, a frog of the Madagascar-Comoroan endemic family Mantellidae, is characterized by a unique internal architecture. Unlike the state commonly observed in anurans, the two discernible olfactory subsystems of M. betsileanus (the main olfactory organ and the vomeronasal organ) are anatomically separated from each other, suggesting an enhanced functional differentiation. Here we evaluate the ontogenetic formation of this extraordinary anatomical state based on a histological study of a developmental series of M. betsileanus. The olfactory system of premetamorphic tadpoles, and most of its changes during metamorphosis, resembles that of other anurans. At the end of metamorphosis however, a growing obstruction of the passage between main olfactory organ and vomeronasal organ takes place, leading to the deviant morphological state previously described for adults. The late appearance of this atypical anatomical feature in the course of ontogeny agrees with the phylogenetic hypothesis of the observed obstruction representing a derived state for these frogs. From a functional point of view, the apparent autonomy of the vomeronasal organ is possibly linked to the presence of clade-specific femoral glands that are known to produce pheromones and that likewise are fully expressed in adults only. Anat Rec, 299:943-950, 2016. © 2016 Wiley Periodicals, Inc.

Volatile compound secretion coincides with modifications of the olfactory organ in mantellid frogs

“…The controlled transport of selected stimuli into the sequestered VNO might be facilitated by specific binding proteins in secretions from the harderian gland or the lateral nasal gland (LNG). The LNG opens directly above the (obstructed) conduit between MOO and VNO in mantellines, at the lateral wall of the nasal cavity (Nowack & Vences, ), similar to the state in frogs with generalized nasal anatomy (Nowack, ). The opening of the nasolacrimal duct into the CM (Fig.…”

“…We studied the anatomy of the olfactory organ of five mantellid species, and compared it with the derived state found in Mantidactylus (Junk et al, 2014;Nowack & Vences, 2016) and with the generalized state found in Rhacophorus (Watanabe, 1936;Junk et al, 2014), a representative of the sister taxon of mantellids.…”

“…The sensory olfactory epithelium is located in the CP (main olfactory organ, MOO) and in a recess of the CI (vomeronasal organ, VNO). A slit‐like opening typically connects CP with CI and CM, but in Mantidactylus it is obstructed and VNO and MOO are separated anatomically (Junk et al ., ), a state developing during metamorphosis (Nowack & Vences, ).…”

The ontogeny of the olfactory system in ceratophryid frogs (Anura, Ceratophryidae)

“…The morphology of the olfactory system in adult stages has been studied in great detail in ranids (Døving, Trotier, Rosin, & Holley, 1993;Gaupp, 1904;McCotter, 1917;Tsui, 1946), in basal anurans (Benzekri & Reiss, 2012;Stephenson, 1951;Wagner, 1934), and in pipids (Dit- surveys across anurans (Helling, 1938;Jurgens, 1971). These studies have shown that the general morphology and organization of this system are shared by the majority of anurans, with the exception of the pipids and ascaphids, in which certain morphological peculiarities have been described as related to the aquatic habits of adults (Paterson, 1951;Reiss & Eisthen, 2008), and in the recently described deviant anatomy of the mantellid Mantidactylus betsileanus (Junk et al, 2014;Nowack & Vences, 2016), where the functional significance appears to relate to perception of femoral gland pheromone secretions (Nowack et al, 2017). The analysis of the adult morphology of the nose in ceratophryid frogs also reveals a somewhat deviant morphology in adult stages of the aquatic Lepidobatrachus spp.…”

Descriptive skeletal anatomy of Blommersia transmarina (Amphibia: Anura: Mantellidae) from the Comoro Islands

“…Increased size of the head in females may indicate an increased cranial volume and vomeronasal organ. This would be a logical evolutionary outcome in view of the transmission of volatile compounds from the males' femoral glands to the females' vomeronasal organ during courtship (Nowack & Vences, 2016;Nowack et al, 2017). Larger sterna and phalanges may likewise aid the female biomechanically in maintaining her vertical position during the reproductive act (Altig, 2008) by increasing muscle attachment area and potentially providing longer input levers relative to output levers.…”