Medullary bone in fossils: function, evolution and significance in growth curve reconstructions of extinct vertebrates

Abstract

Medullary bone (MB) is a special endosteal tissue forming in the bones of female birds during egg laying to serve as a labile calcium reservoir for building the hard eggshell. Therefore, the presence of MB reported in multiple nonavian dinosaurs is currently considered as evidence that those specimens were sexually mature females in their reproductive period. This interpretation has led to further inferences on species-specific growth strategies and related life-history aspects of these extinct vertebrates. However, a few studies questioned the reproductive significance of fossil MB by either regarding the tissue pathological or attributing alternative functions to it. This study reviews the general inferences on extinct vertebrates and discusses the primary role, distribution, regulation and adaptive significance of avian MB to point out important but largely overlooked uncertainties and inconsistencies in this matter. Emerging discordancy is demonstrated when the presence of MB vs. trade-off between growth and reproduction is used for interpreting dinosaurian growth curves. Synthesis of these data suggests that fossil MB was related to high calcium turnover rates but not exclusively to egg laying. Furthermore, revised application of Allosaurus growth data by modelling individual-based growth curves implies a much higher intraspecific variability in growth strategies, including timing of sexual maturation, than usually acknowledged. New hypotheses raised here to resolve these incongruences also propose new directions of research on the origin and functional evolution of this curious bone tissue.

Intraskeletal histovariability, allometric growth patterns, and their functional implications in bird-like dinosaurs

“…As the possible cause of this notably thick ICL has not been discussed in these taxa, it remains unclear whether the extremely thick femoral ICL is pathological or a characteristic feature of the species Jeholornis curvipes . However, a medullary bone origin for this structure is very unlikely, as it lacks the characteristic high porosity and woven bone content of medullary bone 96 , 97 .…”

Medullary bone in an Early Cretaceous enantiornithine bird and discussion regarding its identification in fossils

“…In addition, Chinsamy and Tumarkin-Deratzian 18 showed that tissues remarkably similar to MB occur in some pathological avian bones. Finally, Prondvai and Stein 15 , Chinsamy and colleagues 13 , and Prondvai 19 have reported MBL with unknown functionality in non-pathological and presumably non-reproductive (rapidly growing, juvenile) dinosaurs and pterosaurs. These issues show that caution should be exercised before concluding that MB reflecting sex and reproductive status is truly present in fossils 15 , 18 – 20 .…”

“…The identification of MB in non-avian fossil archosaurs as a means to determine sex and reproductive activity was based on three histological characteristics: (1) location in the medullary cavity; (2) an endosteal origin, marked by a resorption line between the cortex and the hypothetical MB; and (3) a woven arrangement of the collagen fibers, suggesting rapid bone deposition. Given the factors noted above that can produce MBL, these criteria in and of themselves cannot differentiate MB from MBL 18 , 19 . Hence, some past identifications of MB may be incorrect 12 , 20 .…”

“…More precisely, MB is always endosteal in origin (Table 1 ; Criterion 2), but as previously mentioned, it also forms in cancellous spaces of bones without medullary cavities sensu stricto (e.g., in flat bones of the skull, irregular bones like vertebrae) (Criterion 1). Furthermore, recent studies indicate that MB may form more slowly in some large ratites (possibly due to their large size), which has been interpreted as both lamellar 6 , 22 and parallel fibered (Criterion 3) 19 .…”

Estrogen levels influence medullary bone quantity and density in female house finches and pine siskins

“…Changes in circulating hormone levels appear to play an important role in triggering medullary bone formation. Studies focusing on four species belonging to the orders Galliformes, Anseriformes, and Columbiformes have found that elevated estrogen levels stimulate medullary bone formation (Table 1), and it has been presumed that this is the case across the Aves and their recent ancestors (e.g., Prondvai, In press). Yet, these studies reflect a small subset of avian diversity (Fig.…”