Vertebrates have well-organized locomotor appendages (fins and limbs) crucial for environmental adaptation and prosperity. Those locomotor appendages are categorized into two groups based on their location: paired fins (e.g., pectoral, pelvic fins, and limbs) on the bilateral trunk region and unpaired median fins (e.g., caudal, anal, and dorsal fins) along the midline. While median fins are evolutionarily ancestral, it is thought that paired fins evolved by coopting their developmental mechanism to the lateral regions of the body trunk. However, the question of "how a single midline structure was transformed into bilaterally paired structures on the lateral sides" remains unanswered.
To address this question, we focused on the "Twin-tail morphology" observed in certain strains of goldfish and mutant zebrafish. The Twin-tail morphology represents the bilateral duplication of caudal and anal fins, providing a model for analyzing the mechanisms behind the evolutionally developmental transition from midline to bilateral form. In the previous studies, we and other groups found the genetic factors contributing to Twin-tail phenotypes associated with early embryonic ventralization. However, how the ventralization linked to the duplication of the median fins remains unclear. Hence, our study aimed to elucidate the developmental mechanisms responsible for the manifestation of the Twin-tail phenotype by conducting analyses and experiments using zebrafish Twin-tail mutants.
First, we analyzed how the developmental process of the median fin primordia, median fin fold, is altered in Twin-tail embryos through reporter gene expression and cell lineage tracing. Our results revealed that presumptive median fin fold cells in normal embryos expressed broadly and then closed to form a midline single structure. In contrast, in Twin-tail embryos, these cells were more widely distributed and did not close completely. Therefore, it was suggested that the bifurcation of the ventral median fin fold in twin-tail embryos is caused by the movement of the presumptive ventral fin fold cells not closing in the midline due to the influence of early embryonic ventralization. Furthermore, at this time, analysis of the expression of the fin fold marker genes and the functional molecules of fin development revealed that the area capable of fin fold forming expanded from the presumptive ventral fin fold region of the tail to the ventral trunk region. Therefore, it is suggested that the embryonic origin may be shared between the ventral fin fold and the paired fins, at least in the epithelial tissues.
Taken together, our findings suggest that the developmental process of the ventral fin fold intrinsically possesses left-right axis information, and the bilaterality of the ventral fin fold in Twin-tail embryos arises from a failure in the transition from lateral to midline direction. Furthermore, there is a competence field for fin-formation on the ventral side, and it may be that paired fins evolved by directly modifying the developmental mechanism of such a competence shared with median fins.