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How the European eel (Anguilla anguilla) loses its skeletal framework across lifetime.

ABSTRACT: European eels (Anguilla anguilla) undertake an impressive 5 000 km long migration from European fresh waters through the North Atlantic Ocean to the Sargasso Sea. Along with sexual maturation, the eel skeleton undergoes a remarkable morphological transformation during migration, where a hitherto completely obscure bone loss phenomenon occurs. To unravel mechanisms of the maturation-related decay of the skeleton, we performed a multiscale assessment of eels' bones at different life-cycle stages. Accordingly, the skeleton reflects extensive bone loss that is mediated via multinucleated bone-resorbing osteoclasts, while other resorption mechanisms such as osteocytic osteolysis or matrix demineralization were not observed. Preserving mechanical stability and releasing minerals for energy metabolism are two mutually exclusive functions of the skeleton that are orchestrated in eels through the presence of two spatially segregated hard tissues: cellular bone and acellular notochord. The cellular bone serves as a source of mineral release following osteoclastic resorption, whereas the mineralized notochord sheath, which is inaccessible for resorption processes due to an unmineralized cover layer, ensures sufficient mechanical stability as a part of the notochord sheath. Clearly, an eel's skeleton is structurally optimized to meet the metabolic challenge of fasting and simultaneous sexual development during an exhausting journey to spawning areas, while the function of the vertebral column is maintained to achieve this goal.

SUBMITTER: Rolvien T

PROVIDER: S-EPMC5095380 | biostudies-literature | 2016 Oct

REPOSITORIES: biostudies-literature

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How the European eel (Anguilla anguilla) loses its skeletal framework across lifetime.

Rolvien Tim T Nagel Florian F Milovanovic Petar P Wuertz Sven S Marshall Robert Percy RP Jeschke Anke A Schmidt Felix N FN Hahn Michael M Witten P Eckhard PE Amling Michael M Busse Björn B

Proceedings. Biological sciences 20161001 1841

European eels (Anguilla anguilla) undertake an impressive 5 000 km long migration from European fresh waters through the North Atlantic Ocean to the Sargasso Sea. Along with sexual maturation, the eel skeleton undergoes a remarkable morphological transformation during migration, where a hitherto completely obscure bone loss phenomenon occurs. To unravel mechanisms of the maturation-related decay of the skeleton, we performed a multiscale assessment of eels' bones at different life-cycle stages. ...[more]

PMID: 27798301

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Project description:Temperature is important for optimization of rearing conditions in aquaculture, especially during the critical early life history stages of fish. Here, we experimentally investigated the impact of temperature (16, 18, 20, 22 and 24°C) on thermally induced phenotypic variability, from larval hatch to first-feeding, and the linked expression of targeted genes [heat shock proteins (hsp), growth hormone (gh) and insulin-like growth factors (igf)] associated to larval performance of European eel, Anguilla anguilla. Temperature effects on larval morphology and gene expression were investigated throughout early larval development (in real time from 0 to 18 days post hatch) and at specific developmental stages (hatch, jaw/teeth formation, and first-feeding). Results showed that hatch success, yolk utilization efficiency, survival, deformities, yolk utilization, and growth rates were all significantly affected by temperature. In real time, increasing temperature from 16 to 22°C accelerated larval development, while larval gene expression patterns (hsp70, hsp90, gh and igf-1) were delayed at cold temperatures (16°C) or accelerated at warm temperatures (20-22°C). All targeted genes (hsp70, hsp90, gh, igf-1, igf-2a, igf-2b) were differentially expressed during larval development. Moreover, expression of gh was highest at 16°C during the jaw/teeth formation, and the first-feeding developmental stages, while expression of hsp90 was highest at 22°C, suggesting thermal stress. Furthermore, 24°C was shown to be deleterious (resulting in 100% mortality), while 16°C and 22°C (~50 and 90% deformities respectively) represent the lower and upper thermal tolerance limits. In conclusion, the high survival, lowest incidence of deformities at hatch, high yolk utilization efficiency, high gh and low hsp expression, suggest 18°C as the optimal temperature for offspring of European eel. Furthermore, our results suggest that the still enigmatic early life history stages of European eel may inhabit the deeper layer of the Sargasso Sea and indicate vulnerability of this critically endangered species to increasing ocean temperature.

Project description:Gene expression analyses have been performed on brain tissue of sexually mature and immature males using microarrays. 60 eels were transferred to two independent temperature controlled recirculation water units connected to two 500 L cylindro-conical tanks (30 fish per tank) where the fish were acclimated to seawater (35 PSU salinity) over a 2 week period.Eel males in one of the seawater units were injected intramuscularly every week over a 140 day period with 2000 IU hCG/kg (human chorionic gonadotropin, Sigma–Aldrich Chemical) dissolved in 0.9% saline to induce sexual maturation. Eel males in the other recirculation unit were injected weekly over the same period with 0.9% NaCl (vehicle).At the end of the experiment, eels were anesthetized in a solution of 0.1mg/L tricaine methanesulfonate (MS-222, Sigma Aldrich) and blood samples collected into heparinized syringes. Tissues (brain, including the olfactory bulbs, telencephalon, diencephalon and mesencephalon, and gonads) were collected from sexually immature (n=12) and sexually mature males (n=12).RNA was extracted from brain tissue of a total of 24 (12 mature and 12 immature) males. For each individual, RNA was extracted separately for olfactory bulb, telencephalon and diencephalon. Because RNA concentrations of olfactory bulb, telencephalon and diencephalon were below the amount needed for microarray analysis, a separate experiment for each part of the brain was not possible. Therefore, we combined equal concentrations of olfactory bulb, telencephalon and diencephalon as a single brain sample for each individual.Microarray analysis was conducted using an European eel-specific array consisting of a total of 14,913 probes based on a large collection of high-throughput transcriptomic sequences (Pujolar et al. 2012). Probe sequences and further details on the microarray platform can be found on the GEO database under accession number GPL15124. Data was normalized using a quantile normalization procedure using R (http://www.r-project.org)

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How the European eel (Anguilla anguilla) loses its skeletal framework across lifetime.

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How the European eel (Anguilla anguilla) loses its skeletal framework across lifetime.

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