Platyfish bypass the constraint of the caudal fin ventral identity in teleosts

Abstract

Background: The caudal fin of teleosts is characterized by dorsoventral symmetry. Despite this external morphology, the principal rays of this appendage connect to bones below the notochord, indicating the ventral (hypochordal) identity of this organ. Results: Here, we report that this typical architecture of the caudal fin is not fully conserved in the platyfish (Xiphophorus maculatus) and the guppy (Poecilia reticulata), representatives of the Poeciliidae family. We show that in these species, 3–4 principal rays connect to bones above the notochord, suggesting an epichordal contribution. Consistently, as examined in platyfish, dorsal identity genes zic1/4 were highly expressed in these rays, providing molecular evidence of their epichordal origin. Developmental analysis revealed that the earliest rays above the notochord emerge at the 10‐ray stage of fin morphogenesis. In contrast to zebrafish and medaka, platyfish and guppies display a mirrored shape of dorsal and ventral processes of the caudal endoskeleton. Our study suggests that an ancestral bauplan expanded in poeciliids by advancing its symmetrical pattern. Conclusion: The platyfish evolved a fin architecture with the epichordal origin of its upper principal rays and a high level of symmetry in the caudal endoskeleton. This innovative architecture highlights the adaptation of the teleost skeleton.

Regeneration of the dermal skeleton and wound epidermis formation depend on BMP signaling in the caudal fin of platyfish

“…Thus, despite its external dorsoventral symmetry along the midline of the body, the caudal fin can be considered as a ventral appendage. Although this bauplan is highly conserved among teleosts, including the zebrafish and the medaka, we have recently identified a rule-breaking variation in the platyfish ( Xiphophorus maculatus ), a member of the Poeciliidae family of the Cyprinodontiformes order ( Rees et al, 2022 ). This taxon belongs to the Ovalentaria series in neoteleosts, which are considered as modern teleosts, compared to the group represented by zebrafish ( Betancur-R et al, 2017 ) ( Supplementary Figure S1 ).…”

“…This taxon belongs to the Ovalentaria series in neoteleosts, which are considered as modern teleosts, compared to the group represented by zebrafish ( Betancur-R et al, 2017 ) ( Supplementary Figure S1 ). Diverging from the typical anatomical rules of teleosts, the platyfish caudal fin includes principal rays originating from mesenchyme above the notochord, leading to an unconventional dorso-ventral “hybrid” fin ( Rees et al, 2022 ). This finding provides evidence of an unexpected diversity in appendage development among teleosts.…”