Bone metabolism and evolutionary origin of osteocytes: Novel application of FIB-SEM tomography.

Yara Haridy,Donald Davesne,Ingo Manke,Florian Witzmann,André Hilger,Markus Osenberg

doi:10.1126/sciadv.abb9113

Abstract

Lacunae and canaliculi spaces of osteocytes are remarkably well preserved in fossilized bone and serve as an established proxy for bone cells. The earliest bone in the fossil record is acellular (anosteocytic), followed by cellular (osteocytic) bone in the jawless relatives of jawed vertebrates, the osteostracans, about 400 million years ago. Virtually nothing is known about the physiological pressures that would have initially favored osteocytic over anosteocytic bone. We apply focused ion beam-scanning electron microscopy tomography combined with machine learning for cell detection and segmentation to image fossil cell spaces. Novel three-dimensional high-resolution images reveal areas of low density around osteocyte lacunae and their canaliculi in osteostracan bone. This provides evidence for demineralization that would have occurred in vivo as part of osteocytic osteolysis, a mechanism of mineral homeostasis, supporting the hypothesis that a physiological demand for phosphorus was the principal driver in the initial evolution of osteocytic bone.

Highlights

Bone is an essential innovation for all vertebrate life and can undoubtedly be credited for the immense diversity of vertebrate lifestyles; from swimming, to walking, to flying, bone is the material that has provided a literal scaffolding for evolutionary diversity
The isolated osteocyte lacunae and the associated canalicular network in both samples are reminiscent of their modern counterparts in shape and distribution
area of low density (ALD) appears as a dark halo around the lacunae, which contrasts with the grayscale colors of the lacunae and the fossilized bone (Fig. 4)

Summary

Introduction

Bone is an essential innovation for all vertebrate life and can undoubtedly be credited for the immense diversity of vertebrate lifestyles; from swimming, to walking, to flying, bone is the material that has provided a literal scaffolding for evolutionary diversity. The cellular components of bone have been well studied in modern humans in hopes of understanding how to better heal and grow this regenerative tissue [1, 2]. While the developmental relationships of the four cell types (osteoprogenitor, osteoblasts, osteocytes, and osteoclasts) in modern bone are well known [2, 3], very little is known about the evolutionary origins of these cells. Several studies have attributed various physiological roles to osteocytes, including bone remodeling, mechano-sensation, and mineral homeostasis [see [2, 3] and references therein]. The cell lacunae within bone conform so readily to osteocyte shape that the size of these lacunae has been used to estimate genome sizes [5, 6].

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