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Early ontogeny of the olfactory organ in a basal actinopterygian fish: polypterus.

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.

SUBMITTER: Zeiske E

PROVIDER: S-EPMC2746032 | biostudies-literature | 2009

REPOSITORIES: biostudies-literature

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Early ontogeny of the olfactory organ in a basal actinopterygian fish: polypterus.

Zeiske Eckart E Bartsch Peter P Hansen Anne A

Brain, behavior and evolution 20090710 4

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: Acipenser ...[more]

PMID: 19590178

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Project description:While most studies have focused on the timing and nature of ontogenetic niche shifts, information is scarce about the effects of community structure on trophic ontogeny of top predators. We investigated how community structure affects ontogenetic niche shifts (i.e., relationships between body length, trophic position, and individual dietary specialization) of a predatory fish, brown trout (Salmo trutta). We used stable isotope and stomach content analyses to test how functional characteristics of lake fish community compositions (competition and prey availability) modulate niche shifts in terms of (i) piscivorous behavior, (ii) trophic position, and (iii) individual dietary specialization. Northern Scandinavian freshwater fish communities were used as a study system, including nine subarctic lakes with contrasting fish community configurations: (i) trout-only systems, (ii) two-species systems (brown trout and Arctic charr [Salvelinus alpinus] coexisting), and (iii) three-species systems (brown trout, Arctic charr, and three-spined sticklebacks [Gasterosteus aculeatus] coexisting). We expected that the presence of profitable small prey (stickleback) and mixed competitor-prey fish species (charr) supports early piscivory and high individual dietary specialization among trout in multispecies communities, whereas minor ontogenetic shifts were expected in trout-only systems. From logistic regression models, the presence of a suitable prey fish species (stickleback) emerged as the principal variable determining the size at ontogenetic niche shifts. Generalized additive mixed models indicated that fish community structure shaped ontogenetic niche shifts in trout, with the strongest positive relationships between body length, trophic position, and individual dietary specialization being observed in three-species communities. Our findings revealed that the presence of a small-sized prey fish species (stickleback) rather than a mixed competitor-prey fish species (charr) was an important factor affecting the ontogenetic niche-shift processes of trout. The study demonstrates that community structure may modulate the ontogenetic diet trajectories of and individual niche specialization within a top predator.

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Early ontogeny of the olfactory organ in a basal actinopterygian fish: polypterus.

Publications

Early ontogeny of the olfactory organ in a basal actinopterygian fish: polypterus.

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