Abstract
The fish-to-tetrapod transition is one of the fundamental problems in evolutionary biology. A significant amount of paleontological data has revealed the morphological trajectories of skeletons, such as those of the skull, vertebrae, and appendages in vertebrate history. Shifts in bone differentiation, from dermal to endochondral bones, are key to explaining skeletal transformations during the transition from water to land. However, the genetic underpinnings underlying the evolution of dermal and endochondral bones are largely missing. Recent genetic approaches utilizing model organisms—zebrafish, frogs, chickens, and mice—reveal the molecular mechanisms underlying vertebrate skeletal development and provide new insights for how the skeletal system has evolved. Currently, our experimental horizons to test evolutionary hypotheses are being expanded to non-model organisms with state-of-the-art techniques in molecular biology and imaging. An integration of functional genomics, developmental genetics, and high-resolution CT scanning into evolutionary inquiries allows us to reevaluate our understanding of old specimens. Here, we summarize the current perspectives in genetic programs underlying the development and evolution of the dermal skull roof, shoulder girdle, and appendages. The ratio shifts of dermal and endochondral bones, and its underlying mechanisms, during the fish-to-tetrapod transition are particularly emphasized. Recent studies have suggested the novel cell origins of dermal bones, and the interchangeability between dermal and endochondral bones, obscuring the ontogenetic distinction of these two types of bones. Assimilation of ontogenetic knowledge of dermal and endochondral bones from different structures demands revisions of the prevalent consensus in the evolutionary mechanisms of vertebrate skeletal shifts.
Highlights
The fish-to-tetrapod transition during the Devonian is one of the prominent events in vertebrate evolution
Scales that serve as osmotic controls and as protection of the body in an aquatic habitat were lost during landing. With this concomitant loss of dermal bones, the relative ratio of endochondral bones in vertebrae, girdle, and fins increased in early tetrapods
Since the changes of cell origins in cranial dermal bone development across species are summarized in previous studies (Piekarski et al, 2014; Hirasawa and Kuratani, 2015; Maddin et al, 2016), we review current perspectives about molecular pathways that are responsible for cranial dermal bone development with the significant emphasis on interchangeability of dermal and endochondral bones
Summary
The fish-to-tetrapod transition during the Devonian is one of the prominent events in vertebrate evolution. The invasion of the land from the water necessitated the evolution of the novel structures in skeletons, musculatures, innervations, visceral organs, and respiratory systems in order to adapt to a terrestrial life (Romer, 1949; Clack, 2012; Dial et al, 2015). Robust appendage skeletons with associated musculatures evolved to support body weight against gravitational force and to aid with movement on land (Coates, 1996; Shubin et al, 2006). To facilitate respiration in air, gill breathing had transformed to lung breathing through morphological innovations (Zheng et al, 2011; Sagai et al, 2017)
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