Medullary bone-like tissue in the mandibular symphyses of a pterosaur suggests non-reproductive significance

Abstract

Medullary bone is a special bone tissue forming on the endosteal surface of the medullary cavity in the bones of female birds prior to and during egg-laying to serve as a calcium reservoir for building the hard eggshell. It has also been identified in non-avian dinosaurs, where its presence is considered as a reliable indicator of a sexually mature female. Here, we reveal that multiple mandibular symphyses of the azhdarchid pterosaur Bakonydraco galaczi possess a special bone tissue that shows all microanatomical, histological and developmental characteristics of medullary bone, despite its unusual location. Its frequent occurrence in the sample renders a pathologic origin unlikely. Our findings as well as the extremely thin-shelled eggs of pterosaurs suggest that this medullary bone-like tissue probably had a non-reproductive role in these animals. Although the non-reproductive significance and the anatomical location of this medullary bone-like tissue in Bakonydraco suggest independent evolutionary appearance from dinosaurian medullary bone, a common origin and later diverging function and physiological regulation is an equally viable phylogenetic hypothesis.

Introduction

Medullary bone is a non-structural type of bone tissue that, under natural conditions, develops in the haematopoietic medullary cavities of bones of female birds induced by oestrogenic and androgenic hormones during the egg-laying cycle^1,2. Under experimental conditions, administration of these hormones to male birds also results in medullary bone formation^3,4,5. Growing from the endosteal layers inwards to the medullar cavity and mostly being composed of woven bone⁶, medullary bone has no mechanical function but serves as a calcium storage that can be quickly mobilized during the calcification of the hard-shelled eggs of birds^6,7,8,9. According to the phases of the egg-laying cycle, medullary bone can be characterized by rapid formation in the period of maturing follicles and subsequent rapid destruction during the calcification of the eggshell^10,11,12. This fast formation-resorption cycle of medullary bone corresponds well with its microanatomy as well as histology: (i) it has large surface areas due to its highly porous, vascularized nature; (ii) its trabeculae are composed of woven bone⁶; (iii) the number and activity level of osteoclasts is considerably higher in medullary bone than in cortical bone¹³. The composition of medullary bone is similar to that of cortical and cancellous trabecular bone; however, the proportional amount of components are different with medullary bone being more calcified, having higher apatite to collagen ratio and containing more non-collagenous proteins, proteoglycans and carbohydrates in the matrix^7,12,14,15.

This bone tissue type was first described in pigeons¹⁶ and later in some other species of extant birds, among others in domestic fowl, Japanese quail, duck and ostrich^{3,10,11,17,18,19,20,21}. The amount, microanatomy and distribution of medullary bone can be different in different species of birds as well as in different phases of the reproductive cycle^{1,11,17,21,22}. Apart from the controversial results on mice forming medullary bone-like tissues in response to unnaturally high oestrogen doses^23,24, medullary bone has not been reported in any extant non-avian amniotes^25,26. Recently, with the discovery of medullary bone in different non-avian dinosaurs, the occurrence of medullary bone has proven to be phylogenetically more widespread and is considered as further evidence for the close relationship between birds and theropod dinosaurs^21,27,28,29. Apart from dinosaurs, there has been only one report on the presence of an extensive, endosteally derived bone structure in a single femur of the Early Cretaceous pterosaur Pterodaustro that was tentatively interpreted as medullary bone³⁰. Since it has been found in theropod^21,