Comparative data on the differentiation and growth of bone ornamentation in gnathostomes (Chordata: Vertebrata)

Abstract

Bone ornamentation, in the form of rounded pits framed by a network of ridges, is a frequent feature among a great diversity of gnathostome taxa. However, the basic osteogenic processes controlling the differentiation and development of these reliefs remain controversial. The present study is a broad comparative survey of this question with the classical methods used in hard tissue histology and paleohistology. Distinct processes, unevenly distributed among taxa, are involved in the creation and growth of pits and ridges. The simplest one is mere differential growth between pit bottom (slow growth) and ridge top (faster growth). The involvement of several complex remodeling processes, with the local succession of resorption and reconstruction cycles, is frequent and occurs in all major gnathostome clades. Some broad, inclusive clades (e.g., Temnospondyli) display consistency in the mechanisms controlling ornamentation, whereas other clades (e.g., Actinopterygii) are characterized by the diversity of the mechanisms involved. If osteogenic mechanisms are taken into account, bone ornamentation should be considered as a character extremely prone to homoplasy. Maximum likelihood (ML) optimizations reveal that the plesiomorphic mechanism creating ornamentation is differential apposition rate over pits (slow growth) and ridges (faster growth). In some taxas e.g., temnospondyls vs lissamphibians or pseudosuchians, bone ornamentation is likely to be a homoplastic feature due to a convergence process driven by similar selective pressures. ML models of character evolution suggest that the presence of resorption in the development of ornamentation may be selectively advantageous, although support for this conclusion is only moderate.

Cranial bone histology ofMetoposaurus krasiejowensis(Amphibia, Temnospondyli) from the Late Triassic of Poland

“…De Buffrénil et al (2016) observed six main patterns of such modification. The simplest one is repetition of the width or position of pits and ridges from one growth stage to the following one.…”

“…Although dermal sculpture was early recognized as a characteristic of basal tetrapods (e.g., Von Meyer, 1858; Fraas, 1889; Fritsch, 1889; Zittel, 1911), the morphogenesis of the sculptures is still an open question (summarized by Witzmann 2009; Witzmann et al 2010; De Buffrénil et al 2016). Among extant tetrapods, growth of dermal bony tubercles and ridges has been studied in osteoderms of squamates and in dermal skull bones and osteoderms of crocodiles.…”

“…The thin sections of the dermal bones of skull and pectoral girdle in the basal tetrapods investigated by Witzmann (2009) corroborate Bystrow’s findings and show that the dermal sculpture did not develop by local resorption of the bone surface, comparable to the pattern in basal tetrapod osteoderms (Witzmann & Soler-Gijón, 2008). According to the most recent study (De Buffrénil et al, 2016), the involvement of several complex remodeling processes, with the local succession of resorption and reconstruction cycles, is frequent and occurs in all major gnathostome clades, whereas the temnospondyl sections share an important common feature: the lack of superficial remodeling (resorption and reconstruction cycles). However, in the section of Plagiosternum described by Witzmann (2009), the eroded external surface is illustrated.…”

“…Moreover, the study of De Buffrénil et al (2016) showed that, beside the resorption, other dynamics processes also modify the sculpture during bone growth. De Buffrénil et al (2016) observed six main patterns of such modification.…”

“…Later histological studies on the dermal bones in Temnospondyli have focused mainly on morphology and vascular network and collagen fiber organization (Bystrow, 1947; Enlow & Brown, 1956; Coldiron, 1974; De Ricqlès , 1981; Castanet, Francillon-Vieillot & De Ricqlès , 2003; Scheyer, 2007), and were limited only to a few taxa. The systematic studies of dermal bones within numerous tetrapod taxa were provided by Witzmann (2009) and De Buffrénil et al (2016). Up until now, the dermal bones of Metoposaurus have not been studied in detail histologically.…”