The origin of novel features by changes in developmental mechanisms: ontogeny and three‐dimensional microanatomy of polyodontode scales of two early osteichthyans

Abstract

Recent advances in synchrotron imaging allow us to study the three-dimensional (3D) histology of vertebrate fossils, including microfossils (e.g. teeth and scales) of early jawed vertebrates. These microfossils can often be scanned at submicron resolution (<1 µm) because of their small size. The resulting voxel (3D pixel) stacks can be processed into virtual thin sections revealing almost every internal detail of the samples, comparable to traditional thin sections. In addition, 3D models of the internal microanatomical structures, such as embedded odontodes and vasculature, can be assembled and examined in situ. Scales of two early osteichthyans, Psarolepis romeri from the Early Devonian of China and Andreolepis hedei from the Late Silurian of Sweden, were scanned using propagation phase-contrast synchrotron X-ray microtomography (PPC-SRµCT), and 3D models of internal canal systems and buried odontodes were created from the scans. Based on these new data, we review the evolutionary origin of cosmine and its associated pore-canal system, which has been long recognized as a synapomorphy of sarcopterygians. The first odontode that appeared during growth shows almost identical morphology in the two scales, but the second odontode of the Psarolepis scale shows a distinctive morphology with several pores on the surface. It is suggested that a shift from ridge-like odontode to pore-bearing odontode was the key step in the origin of cosmine, which was then elaborated further in more-derived sarcopterygians. We perform a detailed comparison between the two scales and propose a primary homology framework to generate microanatomical characters, which can be used in the phylogenetic analysis of early osteichthyans when more 3D data become available. Our results highlight the importance of 3D data for the study of histology and ontogeny of the dermal skeleton of early jawed vertebrates, especially scales of the polyodontode type. The traditional microvertebrate collection is not only useful for biostratigraphic studies, but also preserves invaluable biological information about the growth of vertebrate hard tissues. Today, we are only beginning to understand the biological meaning of the new 3D data. The increasing availability of such data will enable, and indeed require, a complete revision of traditional palaeohistological studies on early vertebrates.

Three-dimensional paleohistology of the scale and median fin spine ofLophosteus superbus(Pander 1856)

“…The odontodes from a given generation are not in contact with each other, and their contact with the underlying odontodes of the previous generation is mediated by bone of attachment; there is no direct dentine-on-dentine contact. This is different from the pattern of Psarolepis scales and Andreolepis scales, in which the odontodes are in direct contact with each other by dentine, sometimes united by a shared enamel layer, and are added one at a time so that they cannot really be grouped into generations unless you consider each “generation” to contain just one odontode (Qu et al, 2013; Qu et al, 2016). The morphology of first generation odontodes in Lophosteus is similar to the first (primordial) odontode of Andreolepis scales (Qu et al, 2013), with a pointed posterior end and a slender triangular shape.…”

“…In addition, there are several isolated canals that do not connect with any other canals. No such isolated canals are found in Andreolepis or Psarolepis scales (Qu et al, 2016). The horizontal vascular canals are much thicker than those of Andreolepis and Psarolepis scales, especially for the bulbous canals under large young odontodes (Figs.…”

“…Gross (1969) identified Lophosteus as an early osteichthyan that cannot be assigned to either actinopterygians or sarcopterygians, based on the shape and histology of scales and spines. It is the third osteichthyan for which detailed 3D histological data have been obtained from the scales, the other two being Andreolepis (Qu et al, 2013) and Psarolepis (Qu et al, 2016). …”

“…While there is a small amount of directly comparable synchrotron data (Qu et al, 2013; Qu et al, 2016) for the Lophosteus scale, there is no directly comparable 3D data yet published relating to the spine. Soler-Gijón (1999) provided a three-dimensional model of fin spine histology from a xenacanth shark to discuss the structure’s growth, but this was created from a stack of spaced 2D thin sections for which details can sometimes remain uncertain (e.g., osteostracans histology; Qu et al, 2015a).…”

“…General histology terms regarding vertebrate hard tissues follow Francillon-Vieillot et al (1990). The homology assessment of the canal system in 3D follows previous work on the Psarolepis and Andreolepis scales (Qu et al, 2016). …”