The homology and function of the lung plates in extant and fossil coelacanths

Abstract

The presence of a pulmonary organ that is entirely covered by true bone tissue and fills most of the abdominal cavity is hitherto unique to fossil actinistians. Although small hard plates have been recently reported in the lung of the extant coelacanth Latimeria chalumnae, the homology between these hard structures in fossil and extant forms remained to be demonstrated. Here, we resolve this question by reporting the presence of a similar histological pattern–true cellular bone with star-shaped osteocytes, and a globular mineralisation with radiating arrangement–in the lung plates of two fossil coelacanths (Swenzia latimerae and Axelrodichthys araripensis) and the plates that surround the lung of the most extensively studied extant coelacanth species, L. chalumnae. The point-for-point structural similarity of the plates in extant and fossil coelacanths supports their probable homology and, consequently, that of the organ they surround. Thus, this evidence questions the previous interpretations of the fatty organ as a component of the pulmonary complex of Latimeria.

Visualizing mineralization processes and fossil anatomy using synchronous synchrotron X-ray fluorescence and X-ray diffraction mapping

“…Crystallites size extraction show that apatite crystallites from the lung plates yield a homogeneous size of ~10-15 nm, whereas calcite and quartz crystallites are an order of magnitude larger and less uniform in size (~50-150 nm) (figure 2g). This data is totally in accordance with the homogeneity of the ossified, compacted and dense lung plates composed by true cellular bone tissue with osteocytes and globular mineralisation, separated by layers of coarser limestone matrix, observed in thin sections [31,33]. Lung plates of adult specimens of A. araripensis are constituted only by thin layers of homogeneous and compact bone tissue, contrasting to other coelacanth taxa (such as Swenzia latimeriae Clément, 2005) that may display, in addition, a non-mineralised region composed of a collagenic packet of microfibrils [33].…”

“…Such results are illustrated against a millimetre-thick transversal section through superimposed lung plates of the coelacanth A. araripensis (specimen UERJ-PMB 143) from the approximately 110-million-year-old Santana Formation of the Araripe Basin, Brazil (figure 2a). A peculiarity of coelacanths is indeed the presence of a lung covered by ossified plates, described for almost all coelacanth taxa ranging from the Palaeozoic to the Recent [31][32][33][34]. Enriched in yttrium (figure 2b), suggesting an apatite composition [35], these plates are confirmed to be of apatitic bone nature by SRS-XRFD (figure 2c,f ), as previously recognized from the observation of cellular bone with star-shaped osteocytes and a globular mineralization [33].…”

“…Enriched in yttrium (figure 2b), suggesting an apatite composition [35], these plates are confirmed to be of apatitic bone nature by SRS-XRFD (figure 2c,f), as previously recognised from the observation of cellular bone with star-shaped osteocytes and a globular mineralisation [33]. While hardly visible on the optical photograph, elemental and mineralogical maps further show that inner lung plates (i.e.…”

“…A peculiarity of coelacanths is indeed the presence of a lung covered by ossified plates, described for almost all coelacanth taxa ranging from the Palaeozoic to the Recent [31][32][33][34].…”

Ancestral developmental potentials in early bony fish contributed to vertebrate water-to-land transition

“…For instance, the presence of shoulder girdles on the articular surface of the endoskeleton in Late Lochkovian Psarolepis indicates that stem sarcopterygians already possessed an endoskeletal fin pattern similar to that of tetrapod stylopods ( Zhu & Yu, 2009 ). In addition, primitive lungs, which originated from the respiratory pharynx and were located on the ventral side of the alimentary tracts, can be observed in several extant basal actinopterygians (bichirs, reedfish) and all extant sarcopterygians, as well as some fossils of coelacanths and salamanders ( Cupello et al, 2017 ; Tissier et al, 2017 ) ( Figure 1 ). This evidence suggests that, instead of relying on genetic innovations evolving after the first fish left their water habitat, this transition may have been accomplished by adopting physical traits and genetic components that already existed far earlier than when the transition occurred.…”