Pattern of fin rays along the antero-posterior axis based on their connection to distal radials

Abstract

Background Teleost paired fins are composed of two endoskeletal domains, proximal and distal radials, and an exoskeletal domain, the fin ray. The zebrafish pectoral fin displays elaborately patterned radials along the anteroposterior (AP) axis. Radials are considered homologous to tetrapod limb skeletons, and their patterning mechanisms in embryonic development are similar to those of limb development. Nevertheless, the pattern along the AP axis in fin rays has not been well described in the zebrafish pectoral fin, although several recent reports have revealed that fin ray development shares some cellular and genetic properties with fin/limb endoskeleton development. Thus, fin ray morphogenesis may involve developmental mechanisms for AP patterning in the fin/limb endoskeleton, and may have a specific pattern along the AP axis. Results We conducted detailed morphological observations on fin rays and their connection to distal radials by comparing intra- and inter-strain zebrafish specimens. Although the number of fin rays varied, pectoral fin rays could be categorized into three domains along the AP axis, according to the connection between the fin rays and distal radials; additionally, the number of fin rays varied in the posterior part of the three domains. This result was confirmed by observation of the morphogenesis process of fin rays and distal radials, which showed altered localization of distal radials in the middle domain. We also evaluated the expression pattern of lhx genes, which have AP patterning activity in limb development, in fin rays and during distal radial development and found these genes to be expressed during morphogenesis in both fin rays and distal radials. Conclusion The fin ray and its connection to the endoskeleton are patterned along the AP axis, and the pattern along the AP axis in the fin ray and the radial connection is constructed by the developmental mechanism related to AP patterning in the limb/fin bud. Our results indicate the possibility that the developmental mechanisms of fin rays and their connection are comparable to those of the distal element of the limb skeleton.

Morphological evolution and diversity of pectoral fin skeletons in teleosts

“…4F); some anterior distal radials are adjacent to only one fin ray (one-to-one), and other posterior distal radials are adjacent to some fin rays (one- to-many). The same pattern was reported in zebrafish (Hamada et al ., 2019), and the posterior region of zebrafish pectoral fins shows a similar one-to-many pattern as that of sturgeons while the anterior four distal radials are adjacent to fin rays in a one-to-one manner. Pectoral fins in Paracanthopterygii and Acanthopterygii that we observed (Fig.…”

“…Meanwhile, in Tribolodon hakonensis , the anterior distal radials (DR1-4) were connected to fin rays in a one-to-one manner, but the posterior distal radials (DR5-7) were connected to fin rays in a one-to-many manner (Fig. 3I) like the posterior distal radials in zebrafish (Hamada et al ., 2019).…”

“…(3) As for the connection of distal radials and fin rays, zebrafish has one-to-one connections on the anterior side and one-to-many connections on the posterior side (Hamada et al, 2019). On the other hand, African mouthbrooding cichlid seems to have only one-to-one connections (Woltering et al, 2018).…”

“…(2) Regarding the mesocoracoid, some derived teleost species (e.g., African mouthbrooding cichlid) have lost it, while many others retain it (Stiassny, 2000; Helfman et al ., 2009; Hilton, 2011). (3) As for the connection of distal radials and fin rays, zebrafish has one-to-one connections on the anterior side and one-to-many connections on the posterior side (Hamada et al ., 2019). On the other hand, African mouthbrooding cichlid seems to have only one-to-one connections (Woltering et al ., 2018).…”

The genetic basis of coordinated plasticity across functional units in a Lake Malawi cichlid mapping population

“…2018, although see Hamada et al. 2019 for fin ray addition in later juvenile stages). These results underscore the complexity of the pectoral fin, as well as its sensitivity to different types of environmental input, and argue for further investigations into the gene‐by‐environmental interactions that underlie fin morphogenesis and remodeling.…”