New light shed on the early evolution of limb-bone growth plate and bone marrow.

Jordi Estefa,Jozef Klembara,Paul Tafforeau,Grzegorz Niedźwiedzki,Camille Berruyer,Sophie Sanchez,Alice M Clement

doi:10.7554/elife.51581

Abstract

The production of blood cells (haematopoiesis) occurs in the limb bones of most tetrapods but is absent in the fin bones of ray-finned fish. When did long bones start producing blood cells? Recent hypotheses suggested that haematopoiesis migrated into long bones prior to the water-to-land transition and protected newly-produced blood cells from harsher environmental conditions. However, little fossil evidence to support these hypotheses has been provided so far. Observations of the humeral microarchitecture of stem-tetrapods, batrachians, and amniotes were performed using classical sectioning and three-dimensional synchrotron virtual histology. They show that Permian tetrapods seem to be among the first to exhibit a centralised marrow organisation, which allows haematopoiesis as in extant amniotes. Not only does our study demonstrate that long-bone haematopoiesis was probably not an exaptation to the water-to-land transition but it sheds light on the early evolution of limb-bone development and the sequence of bone-marrow functional acquisitions.

Highlights

Tetrapod long bones are among the most studied skeletal elements in the field of bone biology as they constitute a unit of reference for understanding the development and biomechanics of the appendicular skeleton (e.g. Duboule, 1994; Frobisch, 2008; Hall, 2008; Shubin et al, 1997)
The trabecular bone tissues observed in these long bones exhibit characteristics of endochondral ossification as seen in stem- (Sanchez et al, 2014; Sanchez et al, 2016) and crown-tetrapods (Estefa et al, 2020; Francillon-Vieillot et al, 1990; Sanchez et al, 2008; Sanchez et al, 2010a)
The fossils revealed a mineralisation front characterised by a large number of globuli ossei (Figures 2–5), which progressively replaced these hypertrophic chondrocytes, as in urodeles (De Ricqles, 1964; De Ricqles, 1965; Haines, 1938; Quilhac et al, 2014)

Summary

Introduction

Tetrapod long bones are among the most studied skeletal elements in the field of bone biology as they constitute a unit of reference for understanding the development and biomechanics of the appendicular skeleton (e.g. Duboule, 1994; Frobisch, 2008; Hall, 2008; Shubin et al, 1997). Crucial for their biomechanical properties, long bones host bone marrow including stem-cell niches for the production of blood cells, that is haematopoiesis (Orkin and Zon, 2008). Several studies proposed that the skeleton would have played a major role in hosting blood-cell production over the water-to-land transition and (1) protecting it against temperature changes (Weiss and Wislocki, 1956), (2) protecting it against potential DNA mutations induced by UV exposure on land (Horton, 1980; Kapp et al, 2018) or (3) providing a better efficiency in red-blood-cell production necessary for metabolically-demanding terrestrial locomotion and aerial respiration (Tanaka, 1976).

Methods

Results

Conclusion