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Developmental independence of median fins from the larval fin fold revises their evolutionary origin.

ABSTRACT: The median fins of modern fish that show discrete forms (dorsal, anal, and caudal fins) are derived from a continuous fold-like structure, both in ontogeny and phylogeny. The median fin fold (MFF) hypothesis assumes that the median fins evolved by reducing some positions in the continuous fin fold of basal chordates, based on the classical morphological observation of developmental reduction in the larval fin folds of living fish. However, the developmental processes of median fins are still unclear at the cellular and molecular levels. Here, we describe the transition from the larval fin fold into the median fins in zebrafish at the cellular and molecular developmental level. We demonstrate that reduction does not play a role in the emergence of the dorsal fin primordium. Instead, the reduction occurs along with body growth after primordium formation, rather than through actively scrapping the non-fin forming region by inducing cell death. We also report that the emergence of specific mesenchymal cells and their proliferation promote dorsal fin primordium formation. Based on these results, we propose a revised hypothesis for median fin evolution in which the acquisition of de novo developmental mechanisms is a crucial evolutionary component of the discrete forms of median fins.

SUBMITTER: Miyamoto K

PROVIDER: S-EPMC9079066 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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Developmental independence of median fins from the larval fin fold revises their evolutionary origin.

Miyamoto Kazuhide K Kawakami Koichi K Tamura Koji K Abe Gembu G

Scientific reports 20220507 1

The median fins of modern fish that show discrete forms (dorsal, anal, and caudal fins) are derived from a continuous fold-like structure, both in ontogeny and phylogeny. The median fin fold (MFF) hypothesis assumes that the median fins evolved by reducing some positions in the continuous fin fold of basal chordates, based on the classical morphological observation of developmental reduction in the larval fin folds of living fish. However, the developmental processes of median fins are still unc ...[more]

PMID: 35525860

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Project description:The evolution of the tetrapod limb involved an expansion and elaboration of the endoskeletal elements, while the fish fin rays were lost. Loss of fin-specific genes, and regulatory changes in key appendicular patterning genes have been identified as mechanisms of limb evolution, however their contributions to cellular organization and tissue differences between fins and limbs remains poorly understood. During early larval fin development, hoxa13a/hoxd13a-expressing fin fold mesenchyme migrate through the median and pectoral fin along actinotrichia fibrils, non-calcified skeletal elements crucial for supporting the fin fold. Fin fold mesenchyme migration defects have previously been proposed as a mechanism of fin dermal bone loss during tetrapod evolution as it has been shown they contribute directly to the fin ray osteoblast population. Using the nitroreductase/metronidazole system, we genetically ablated a subset of hoxa13a/hoxd13a-expressing fin fold mesenchyme to assess its contributions to fin development. Following the ablation of fin fold mesenchyme in larvae, the actinotrichia are unable to remain rigid and the median and pectoral fin folds collapse, resulting in a reduced fin fold size. The remaining cells following ablation are unable to migrate and show decreased actinodin1 mesenchymal reporter activity. Actinodin proteins are crucial structural component of the actinotrichia. Additionally, we show a decrease in hoxa13a, hoxd13a, fgf10a and altered shha, and ptch2 expression during larval fin development. A continuous treatment of metronidazole leads to fin ray defects at 30dpf. Fewer rays are present compared to stage-matched control larvae, and these rays are shorter and less defined. These results suggest the targeted hoxa13a/hoxd13a-expressing mesenchyme contribute to their own successful migration through their contributions to actinotrichia. Furthermore, due to their fate as fin ray osteoblasts, we propose their initial ablation, and subsequent disorganization produces truncated fin dermal bone elements during late larval stages.

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Developmental independence of median fins from the larval fin fold revises their evolutionary origin.

Publications

Developmental independence of median fins from the larval fin fold revises their evolutionary origin.

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