Early Ontogeny of the Olfactory Organ in a Basal Actinopterygian Fish: <i>Polypterus</i>

Abstract

The present study employed light and electron microscopic methods to investigate the ontogenetic origin of the olfactory organ in bichirs (Cladistia: Polypteridae) and explore its evolution among osteichthyans. In former studies we demonstrated that in teleosts a subepidermal layer gives rise to the olfactory placode which in turn builds all types of olfactory cells (basal, receptor, supporting, ciliated non-sensory cells). In contrast, the olfactory placodes in sturgeons (Chondrostei: Acipenseridae) as well as in the clawed frog Xenopus laevis (Anura: Pipidae) originate from two different layers. Receptor neurons derive from cells of the subepidermal (sensory) layer and supporting cells from epidermal cells. As sturgeons and amphibians in some characters show a more primitive condition than teleosts, we extended our study to Polypterus to allow for an approach at the basic osteichthyan pattern. In Polypterus, an internal lumen occurs in early ontogenetic stages surrounded by the epithelium of the olfactory placode. Two different populations of supporting cells follow one another: a primary population derives from the subepidermal layer. Later supporting cells develop from epidermal cells by transdifferentiation. The primary opening of the internal lumen to the exterior develops by invagination from the epidermal surface and simultaneously by a counter-directed process of cell dissociation and fragmentation inside the olfactory placode. Our results indicate the following features to be plesiomorphic actinopterygian character states: The primary olfactory pit (prospective olfactory cavity) is formed by invagination of the epidermal and the subepidermal layer (as in Acipenser and Xenopus). The incurrent and excurrent nostrils derive from a single primary opening which elongates and is then separated by an epidermal bridge into the two external openings (as in Acipenser and many teleosts). The olfactory epithelium derives from an epidermal and a subepidermal layer (as in Acipenser and Xenopus). Apomorphic (derived actinopterygian) features are: (1) an internal lumen as primordium of the future olfactory chamber; (2) a subepidermal layer gives rise to the olfactory epithelium and its constituents (Polypterus and teleosts). As to the origin of the olfactory supporting cells in Polypterus we assume a combination of plesiomorphic and apomorphic characters. We conclude that Acipenser and Xenopus exhibit the most widely distributed features among basal osteognathostomes and thus ancestral character states in the development of the olfactory organs.

Immunohistochemical distribution of calretinin and calbindin (D‐28k) in the brain of the cladistian Polypterus senegalus

“…The sensory olfactory epithelium of adult cladistians consists of basal, supporting, and ciliated nonsensory cells, and three types of ORNs: ciliated, microvillous, and crypt cells (Schulte and Holl, 1971;Zeiske et al, 2009). The present results reveal CR immunoreaction in some ORNs of the olfactory mucosa in Polypterus senegalus, which showed a clear zonal distribution near the basis in all lamellae, and most of these neurons probably bear cilia (ciliary ORNs).…”

Polypteridae (Actinopterygii: Cladistia) and DANA-SINEs insertions

“…Actually, African Polypterids include only two genera (Gosse, 1984;Greenwood, 1984;Gayet et al, 2001;Otero et al, 2006): Erpetoichthys, with the unique species of E. calabaricus, and Polypterus, with 16 different formally described species (Schafer, 2004;Britz, 2004;Schliewen and Schafer, 2006). These interesting species shows both symplesiomophies with other basal actinonopterygian groups, than new synapomophies or convergent features (Zeiske et al, 2009). The systematic position of the species belonging to the Polypteriformes have been debated for a long time (Noack et al, 1996;Zardoya and Meyer, 1996;Daget et al, 2001;Ledje et al, 2002;Bagrosky et al, 2003;Britz and Johnson, 2003;Gardiner et al, 2005;Mallatt and Winchell, 2007;Morescalchi et al, 2007Morescalchi et al, , 2008, but currently they are considered to be the most basal Actinopterygyans, the Cladistia (Venkatesh et al, 1999(Venkatesh et al, , 2001Britz and Bartsch, 2003;Kikugawa et al, 2004;Claeson et al, 2007), also if still remain poorly understood the intraspecific diversification and the interrelationships among the ten extant African Polypterus species (Hanssens et al, 1995;Gayet et al, 2001;Daget et al, 2001;Britz, 2004;Otero et al, 2006).…”

Olfactory Sensory Neuron Morphotypes in the Featherback Fish, Notopterus notopterus (Osteoglossiformes: Notopteridae)

“…These are however widespread in number of teleost fishes. 10,12,58,59,62-66 They are reported in Cyprinodonts, 37 catfish, swordtail and needlefishes 11 and in Zebrafish, Danio rerio . 13 …”

“…57 In addition to the teleosts, expression of both ciliated and microvillous sensory cells is seen in a primitive extant ray-finned fishes, the bichir ( Polypterus senegalus and P. ornatipinnis 58 ) and the sturgeons of genus Acipencer. 59 They occur together but in varying proportions in different species.…”