Bone mineral density reduction explains buoyancy adaptations in notothenioids

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In aquatic vertebrates, dense skeletons and buoyant fat constitute important components for buoyancy regulation in addition to their roles in structural support and energy storage. Some fishes can fine-tune buoyancy using their swim bladder, whereas others rely on neutral buoyancy or constant motion to regulate vertical position. The Notothenioidei provides a model system to study the phenotypic implications of differential use of the water column over a large radiation of closely related species. It has been suggested that to expand from ancestral benthic to pelagic habitats, some notothenioids, all of which lack the swim bladder, have reduced skeletal mass and display enhanced lipid deposition. This, apparently, adaptive osteopenia has interesting medical implications in understanding the balance between osteopenic bone and structural integrity of the skeleton.

While relative buoyancy in seawater (%B) and dry skeletal mass have previously been studied in some notothenioids, little is known about the specific anatomical changes resulting in osteopenia; hypotheses include reductions of bone mineralization, reductions in bone size, and/or modifications of bone architecture. Here we used a high-throughput procedure relying on quantitative X-ray computed tomography (qCT) imaging on a collection of 436 notothenioid specimens (7 families, 24 genera, 53 species) to measure overall volumetric bone mineral density (vBMD), body size-adjusted mineral content of the entire skeleton (BMCtotal), vertebrae (BMCvertebrae), and skull bones (BMCskull), and body size adjusted lipid content (LC). Dual-energy X-ray absorptiometry and magnetic resonance imaging on a subsample of 50 specimens was used for BMCtotal and LC validation.

For 33 species in the collection, %B was available from the literature and we performed phylogenetic generalized least-squares analysis with seven models to explain buoyancy (%B ~ BMCtotal, %B ~ BMCskull, %B ~ BMCvertebrae, %B ~ BMCtotal + BMCskull, %B ~ BMCtotal + BMCvertebrae, %B ~ BMCtotal + BMCskull + BMCvertebrae, %B ~ LC). This phylogenetically informed multivariate data analysis showed that the model %B ~ BMCtotal + BMCvertebrae best described the data, thus evolutionary reductions in %B are best explained by reductions in both BMCtotal and BMCvertebrae.

In a series of studies, Eastman et al. established the link between buoyancy, skeletal mass, and LC in notothenioids, most recently in a comprehensive report spanning 54 specimens of 20 species (Eastman et al. J Morphol. 2014, 275:841–61). The present result confirms on a much broader scale the correlation between bone mineral content and buoyancy, and shows that vertebrae are the most important bone type for overall reductions in BMC. Based on qCT, micro-CT, histology, and mechanical testing, we seek to answer to which extend the reduction in BMC compromises the mechanical integrity of the bone.
OriginalsprogEngelsk
TidsskriftF A S E B Journal
Vol/bind33
Nummer1
ISSN0892-6638
StatusUdgivet - 2019

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