3D morphological analysis of spiral intestine morphogenesis in the little skate, Leucoraja erinacea

Abstract

Background The evolution of organ asymmetries is less explored than the field of organ morphology and coiling. The digestive tract of elasmobranchs provides a fascinating model for studying the evolution of morphological asymmetries. Unique to elasmobranchs and all basal fishes is the spiral intestine, which may represent an intermediate morphology in evolution from the straight gut of lamprey to the elongated coils of higher vertebrates. The short spiral allows for a large absorptive surface area that can fit into a restrictive abdominal space. Results Using histology and high resolution microCT, we provide the first 3D morphometric analysis of the spiral intestine during development in the little skate, Leucoraja erinacea. Spiral formation is initiated by asymmetric growth in the mesenchyme, causing a bulging fold that protrudes into the lumen of the gut. As development proceeds, the fold elongates and spirals into a right‐handed helix. Spiraling progresses along the anterior‐posterior axis and is likely the result of mechanical forces driven by the asymmetric growth of surrounding tissues. After initial asymmetric growth, radial constraints from within the gut tube create constrictive forces further propagating spiraling. Conclusion We propose a model for potential biophysical mechanisms that direct the morphogenesis of the spiral intestine.

Phosphotungstic acid‐enhanced microCT: Optimized protocols for embryonic and early postnatal mice

“…Further experimentation could broaden the application of this protocol across mammalian and non‐mammalian species for which microCT studies are becoming more common. For example, this protocol could be combined with PaxGene fixation protocols to both preserve the ability for RNA extraction while improving contrast within soft tissue structures or potentially be applied to non‐mammalian species in which contrast‐enhanced microCT has been increasingly utilized to study development of soft tissue structures . Overall, the combination of detailed protocols for staining tissues with PTA and wax embedding to minimize tissue shrinkage and movement artifacts during scanning has broad applications.…”

“…For example, this protocol could be combined with PaxGene fixation protocols to both preserve the ability for RNA 46,47 or potentially be applied to nonmammalian species in which contrast-enhanced microCT has been increasingly utilized to study development of soft tissue structures. 2,40,41,48 Overall, the combination of detailed protocols for staining tissues with PTA and wax embedding to minimize tissue shrinkage and movement artifacts during scanning has broad applications.…”

Non‐model organisms and unique approaches are needed for the future of evo‐devo

“…Their findings suggest that FoxA may be a late evolutionary acquisition of chordates. Another study, by Theodosiou and Oppong, demonstrates how the study of spiral intestine development in the little skate is a good model system to study the evolution of morphological asymmetries. A review article discussing the mechanisms of cardiac development across taxa (cephalopods, insects and beyond) reveals that understanding the evolutionary history of the cardiac system from a developmental perspective provides important insights into congenital cardiac malformations in humans .…”

“…The papers in this Special Issue are no exception to this rule. High resolution micro CT is applied to generate a 3‐D morphometric dataset documenting the developmental progression of the spiral in the little skate's intestine . The latest scanning electron microscopy technologies, which allow high resolution imaging of large areas, is combined with digital imaging and automated image analyses to study the ultrastructural diversity of butterfly wing scales .…”

“…Their findings suggest that FoxA may be a late evolutionary acquisition of chordates. Another study, by Theodosiou and Oppong, 5 demonstrates how the study of spiral intestine development in the little skate is a good model system to study the evolution of morphological asymmetries.…”