Growth dynamics and molecular bases of evolutionary novel jaw extensions in halfbeaks and needlefishes (Beloniformes)

Abstract

Evolutionary novelties—derived traits without clear homology found in the ancestors of a lineage—may promote ecological specialization and facilitate adaptive radiations. Examples for such novelties include the wings of bats, pharyngeal jaws of cichlids and flowers of angiosperms. Belonoid fishes (flying fishes, halfbeaks and needlefishes) feature an astonishing diversity of extremely elongated jaw phenotypes with undetermined evolutionary origins. We investigate the development of elongated jaws in a halfbeak ( Dermogenys pusilla ) and a needlefish ( Xenentodon cancila ) using morphometrics, transcriptomics and in situ hybridization. We confirm that these fishes' elongated jaws are composed of distinct base and novel ‘extension’ portions. These extensions are morphologically unique to belonoids, and we describe the growth dynamics of both bases and extensions throughout early development in both studied species. From transcriptomic profiling, we deduce that jaw extension outgrowth is guided by populations of multipotent cells originating from the anterior tip of the dentary. These cells are shielded from differentiation, but proliferate and migrate anteriorly during the extension's allometric growth phase. Cells left behind at the tip leave the shielded zone and undergo differentiation into osteoblast‐like cells, which deposit extracellular matrix with both bone and cartilage characteristics that mineralizes and thereby provides rigidity. Such bone has characteristics akin to histological observations on the elongated ‘kype’ process on lower jaws of male salmon, which may hint at common conserved regulatory underpinnings. Future studies will evaluate the molecular pathways that govern the anterior migration and proliferation of these multipotent cells underlying the belonoids' evolutionary novel jaw extensions.