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)

Abstract

Nearly all vertebrates possess an olfactory organ but the vomeronasal organ is a synapomorphy for tetrapods. Nevertheless, it has been lost in several groups of tetrapods, including aquatic and marine animals. The present study examines the development of the olfactory and vomeronasal organs in two terrestrial anurans that exhibit different developmental modes. This study compares the development of the olfactory and vomeronasal organs in metamorphic anurans that exhibit an aquatic larva (Bufo americanus) and directly developing anurans that have eliminated the tadpole (Eleutherodactylus coqui). The olfactory epithelium in larval B. americanus is divided into dorsal and ventral branches in the rostral and mid-nasal regions. The larval olfactory pattern in E. coqui has been eliminated. Ontogeny of the olfactory system in E. coqui embryos starts to vary substantially from the larval pattern around the time of operculum development, the temporal period when the larval stage is hypothesized to have been eliminated. The nasal anatomy of the two frogs does not appear morphologically similar until the late stages of embryogenesis in E. coqui and the terminal portion of metamorphosis in B. americanus. Both species and their respective developing offspring, aquatic tadpoles and terrestrial egg/embryos, possess a vomeronasal organ. The vomeronasal organ develops at mid-embryogenesis in E. coqui and during the middle of the larval period in B. americanus, which is relatively late for neobatrachians. Development of the vomeronasal organ in both frogs is linked to the developmental pattern of the olfactory system. This study supports the hypothesis that the most recent common ancestor of tetrapods possessed a vomeronasal organ and was aquatic, and that the vomeronasal organ was retained in the Amphibia, but lost in some other groups of tetrapods, including aquatic and marine animals.

Immunohistochemical localization of vascular endothelial growth factor and its receptor Flk-1 in the amphibian developing principal and accessory olfactory system

“…At present, a complete description of the VN system in Bufo arenarum has not been documented. However, our observations demonstrated that the development and structures of the principal and accessory olfactory systems are similar to those recently described for B. americanus (Jermakowicz III et al 2004).…”

Ontogeny of the somatostatin variant [Pro2,Met13]somatostatin-14 in the brain, pituitary, and sensory organs of the frogRana esculenta

“…PSS2 54-66 -like immunoreactivity was also visualized from stages IV-VII onward in the vomeronasal organ, in the accessory olfactory bulb, and in the taste buds of the oral cavity. These observations indicate that, during ontogeny, SS2 may affect the function of these sensorial systems which have an important role in mediating unconditioned and reinforcing properties of natural chemicals (Osculati and Sbarbati, 1995;Jermakowicz et al, 2004).…”

Ontogeny of central serotonergic neurons in the directly developing frog, Eleutherodactylus coqui

“…Callery and Elinson (2000b) proposed that the period between TS 9 and TS 12 represents a time where the deletion of the tadpole from the ancestral, biphasic lifehistory occurred. During this period of development in the larval olfactory organ, a configuration observed in metamorphic frogs, has been eliminated in E. coqui (Jermakowicz et al 2004). Interestingly, during this period the serotonergic system undergoes a slow and gradual growth in E. coqui.…”

“…This frog exhibits many developmental modifications from the metamorphic anuran pattern including: repatterned skull development (Hanken et al 1992), modified operculcum development and ontogenetic reorganization (Callery and Elinson 2000b), absence of the larval olfactory organs (Jermakowicz et al 2004), early thyroid gland development (Jennings and Hanken 1998), and a T 3 -dependent developmental period, similar to what occurs during metamorphosis (Callery and Elinson 2000a; for reviews see Hanken 1999;Callery et al 2001;Elinson 2001).…”