Cellular and molecular mechanisms of frontal bone development in spotted gar (Lepisosteus oculatus)

Abstract

AbstractBackgroundThe molecular mechanisms initiating vertebrate cranial dermal bone formation is a conundrum in evolutionary and developmental biology. Decades of studies have determined the developmental processes of cranial dermal bones in various vertebrate species, finding possible inducers of dermal bone. However, the evolutionarily derived characters of current experimental model organisms hinder investigations of the ancestral and conserved mechanisms of vertebrate cranial dermal bone induction. Thus, investigating such mechanisms with animals diverging at evolutionarily crucial phylogenetic nodes is imperative.ResultsWe investigated the cellular and molecular foundations of skull frontal bone formation in the spotted gar Lepisosteus oculatus, a basally branching actinopterygian. Whole-mount bone and cartilage stainings and hematoxylin-eosin section stainings revealed that mesenchymal cell condensations in the frontal bone of spotted gar develop in close association with the underlying cartilage. We also identified novel aspects of frontal bone formation: Upregulation of F-actin and plasma membrane in condensing cells, and extension of podia from osteoblasts to the frontal bone, which may be responsible for bone mineral transport.ConclusionThis study highlights the process of frontal bone formation with dynamic architectural changes of mesenchymal cells in spotted gar, illuminating supposedly ancestral and likely conserved developmental mechanisms of skull bone formation among vertebrates.