The inner ear of gymnophione amphibians and its nerve supply: A comparative study of regressive events in a complex sensory system (Amphibia, Gymnophiona)

Abstract

The inner ears of representatives of all six gymnophionan families, as well as an ontogenetic series of one species, were studied in order to understand the origin and changes of the amphibian and basilar papillae. The amphibian papilla is in close proximity to the papilla neglecta in some adult gymnophionans. During ontogeny, both epithelia are adherent before they are separated by the formation of the utriculosaccular foramen. The nerve fibers to both epithelia run together, and both epithelia show a comparable variation in size and position among amphibians (amphibian papilla) and among vertebrates (papilla neglecta). Based on these arguments we propose that the amphibian papilla is a translocation of a part of the papilla neglecta specific to amphibians. Present in all primitive gymnophionans, the basilar papilla is lost in all derived gymnophionans. In contrast to anurans, but similar to some urodeles, amniotes, and Latimeria, the basilar papilla rests partly on a basilar membrane. Because of similarities in structure, topology, and innervation, the basilar papilla is suggested to be homologous in Latimeria and tetrapods. The structural differences of most amphibian basilar papillae, compared to those of amniotes and Latimeria, may be due to the different course of the periotic system and the formation of a basilar papillar recess rather than to a separate evolution of this epithelium. In addition to loss of the basilar papilla, some derived gymnophionans have lost the lagena, presumably independently, and the amphibian papilla is extremely reduced in the only genus without a stapes (Scolecomorphus). The papilla neglecta is, for unknown functional reasons, relatively large in aquatic gymnophionans, whereas it is almost lost in some thoroughly terrestrial gymnophionans. The regressive changes in the inner ear are not reflected in obvious changes in the pattern of eighth nerve projection. However, there is a rearrangement of cell masses in the rhombencephalic alar plate of derived gymnophionans, which may be related to the partial or complete loss of lateral line afferents. We propose that the presence of a basilar papilla is a synapomorphy of tetrapods and Latimeria, that the translocation of the papilla neglecta is related to the unique course of the amphibian periotic canal, and that regressive changes in the inner ear are related to the primitive absence of a tympanic ear.