Development and growth of the pectoral girdle and fin skeleton in the extant coelacanthLatimeria chalumnae

Abstract

The monobasal pectoral fins of living coelacanths and lungfishes are homologous to the forelimbs of tetrapods and are thus critical to investigate the origin thereof. However, it remains unclear whether the similarity in the asymmetrical endoskeletal arrangement of the pectoral fins of coelacanths reflects the evolution of the pectoral appendages in sarcopterygians. Here, we describe for the first time the development of the pectoral fin and shoulder girdle in the extant coelacanth Latimeria chalumnae, based on the tomographic acquisition of a growth series. The pectoral girdle and pectoral fin endoskeleton are formed early in development with a radially outward growth of the endoskeletal elements. The visualization of the pectoral girdle during development shows a reorientation of the girdle between the fetus and pup 1 stages, creating a contact between the scapulocoracoids and the clavicles in the ventro‐medial region. Moreover, we observed a splitting of the pre‐ and post‐axial cartilaginous plates in respectively pre‐axial radials and accessory elements on one hand, and in post‐axial accessory elements on the other hand. However, the mechanisms involved in the splitting of the cartilaginous plates appear different from those involved in the formation of radials in actinopterygians. Our results show a proportional reduction of the proximal pre‐axial radial of the fin, rendering the external morphology of the fin more lobe‐shaped, and a spatial reorganization of elements resulting from the fragmentation of the two cartilaginous plates. Latimeria development hence supports previous interpretations of the asymmetrical pectoral fin skeleton as being plesiomorphic for coelacanths and sarcopterygians.

Cranial or postcranial—Dual origin of the pectoral appendage of vertebrates combining the fin‐fold and gill‐arch theories?

“…In fact, there is only one living taxon where the pectoral fin does have such a striking resemblance with the median fins, the coelacanth Latimeria , 60‐61 and such a striking likeness has been argued to be likely due to a homeotic transformation 62 . However, the simple fact that—even if this mainly only happens in Latimeria —an homeotic transformation was likely involved in a phenotype where the adult pectoral fin is so strikingly similar to the pelvic fin and the other fins might in fact be used by those supporting the fin‐fold theory.…”

Development and growth of the pelvic fin in the extant coelacanthLatimeria chalumnae

“…As for the pectoral fin of L . chalumnae (Mansuit et al, 2019), we use the term mesomere for subcylindrical radial segments of the principal axis in sarcopterygian fins (Jarvik, 1980).…”

“…The organization of the radial elements along the metapterygial axis is similar on the pelvic fin and on the pectoral fin, except for the presence of a preaxial radial (called preaxial radial 0) on the pelvic fin only (Figure 7). As in the pectoral fin (Mansuit et al, 2019; Millot & Anthony, 1958) there is an important difference in morphology of the preaxial radial elements between the most proximal elements (pr.rad. 0–2) and the distal elements (pr.rad.…”

“…Indeed, only a few embryos and one juvenile are present in collections worldwide (Nulens, Scott, & Herbin, 2011). Due to the improvement of noninvasive imaging techniques such as conventional and synchrotron micro‐tomography, as well as magnetic resonance imaging, it is now possible to study the development of small and complex internal structures of the coelacanth like the lung (Cupello et al, 2015), the neurocranium (Dutel et al, 2019) and the pectoral fin (Mansuit et al, 2019).…”

“…The endoskeleton elements of the paired fins or limbs are organized along a single metapterygial axis in sarcopterygians (Millot & Anthony, 1958; Shubin & Alberch, 1986). However, whereas the development of paired appendages in lungfishes and tetrapods is relatively well known (Boisvert, Joss, & Ahlberg, 2013; Jude, Johanson, Kearsley, & Friedman, 2014; Shubin & Alberch, 1986), it remains poorly studied in coelacanths (but see (Mansuit et al, 2019). Yet, the development of the pelvic appendages of vertebrates occurs later than the pectoral appendages (Cubbage & Mabee, 1996; Mabee & Noordsy, 2004; Mabee & Trendler, 1996).…”