Identifying medullary bone in extinct avemetatarsalians: challenges, implications and perspectives

Abstract

Medullary bone (MB) is a sex-specific tissue produced by female birds during the laying cycle, and it is hypothesized to have arisen within Avemetatarsalia, possibly outside Avialae. Over the years, researchers have attempted to define a set of criteria from which to evaluate the nature of purported MB-like tissues recovered from fossil specimens. However, we argue that the prevalence, microstructural and chemical variability of MB in Neornithes is, as of yet, incompletely known and thus current diagnoses of MB do not capture the extent of variability that exists in modern birds. Based on recently published data and our own observations of MB distribution and structure using computed tomography and histochemistry, we attempt to advance the discourse on identifying MB in fossil specimens. We propose: (i) new insights into the phylogenetic breadth and structural diversity of MB within extant birds; (ii) a reevaluation and refinement of the most recently published list of criteria suggested for confidently identifying MB in the fossil record; (iii) reconsideration of some prior identifications of MB-like tissues in fossil specimens by taking into account the newly acquired data; and (iv) discussions on the challenges of characterizing MB in Neornithes with the goal of improving its diagnosis in extinct avemetatarsalians. This article is part of the theme issue ‘Vertebrate palaeophysiology’.

Assessing ontogenetic maturity in extinct saurian reptiles

“…medullary bone), and similar tissues have been reported in many stem avians, prompting interpretations of these individuals as being sexually mature (Schweitzer, Wittmeyer & Horner, 2005; Lee & Werning, 2008; Hübner, 2012; Chinsamy et al ., 2013). Although the interpretation of certain tissues as medullary bone in the fossil record remains controversial (Chinsamy & Tumarkin‐Deratzian, 2009; Prondvai & Stein, 2014; Griffin, 2019 b ; reviewed by Prondvai, 2017; Canoville et al ., 2020), a consensus has been forming on the phylogenetic extent and proper diagnostic criteria of this tissue (Canoville et al ., 2020). Because medullary bone is not expected to be present in males or in females in a different stage of the egg‐laying cycle, the absence of medullary bone does not entail sexual immaturity.…”

“…Raath, 1990; Klein & Sander, 2008; Saitta, 2015; Griffin & Nesbitt, 2016 a , b ), population structure and taphonomy (Badgley, 1986; Erickson et al ., 2009 a , 2010), heterochrony (Gould, 1977; Bhullar et al ., 2012), and reproductive biology (e.g. Lee & Werning, 2008; Canoville, Schweitzer & Zanno, 2020) can be inferred across lineages with long evolutionary histories. Assessing maturity is one of the first steps in identifying a species, and all other palaeobiological and evolutionary hypotheses are built on this initial interpretation.…”

Vertebrate palaeophysiology

“…The contributions of Canoville et al [2] and Huttenlocker & Shelton [11] provide insights into early growth and life cycle innovations of avianline archosaurs and synapsids, respectively. In addition to discussing the typology and histochemistry of medullary bone, Canoville et al promote its use towards understanding more generally the fascinating reproductive biology of dinosaurs [2]. Better characterization of medullary tissues in reproductive dinosaurs would help palaeontologists identify sexual dimorphism in the fossil record, more accurately estimate growth rate and age at maturity, and understand nesting and rearing behaviour.…”

“…'Vertebrate palaeophysiology' will promote a better understanding of how organism-environment interactions have evolved in terms of energy budgets, predator-prey relationships and sensitivity to environmental change. The research areas covered by this theme issue include: phospho-calcic metabolism [2], acid-base homeostasis [3,4], thermometabolism [4][5][6][7][8][9], respiratory physiology [10], skeletal growth [11], palaeopathophysiology [12,13], genome size and metabolic rate [14], and a concluding historical perspective [15]. Sometimes, the two components ( physiological mechanism and palaeobiological inference) are proposed in separate papers (for instance, three contributions devoted to mechanisms of thermogenesis mechanisms [5][6][7] and three papers dealing with the thermometabolic inferences in extinct taxa [4,8,9]).…”

Keratan sulfate as a marker for medullary bone in fossil vertebrates

“…This indicates that most sampled pathologies contained detectable amounts of glycosaminoglycans and moreover, that these histochemical staining methods are not adequate to discriminate between medullary bone and structurally similar, endosteally-derived pathological tissues. In fact, chemical staining protocols with Alcian blue and HID used in this study are standard methodologies for localizing high concentrations of glycosaminoglycans in the matrix of cartilage and bone tissues of extant vertebrates (Bailleul et al, 2020;Canoville et al, 2019Canoville et al, , 2020aPage & Ashhurst, 1987;Sobue & Takeuchi, 1979;Yamamoto et al, 2005).…”