Ancestral developmental potentials in early bony fish contributed to vertebrate water-to-land transition.

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The water-to-land transition was a major step in vertebrate evolution and eventually gave rise to the tetrapods, including amphibians, reptiles, birds, and mammals. The first land invasion of our fish ancestors is considered to have occurred during the late Devonian period ~370 million years ago (Mya) (Daeschler et al., 2006). Many fossils from important transitional species, such as Tiktaalik, Acanthostega, and Ichthyostega, have helped to identify key morphological and anatomical structures crucial to vertebrate terrestrial adaptation (Coates, 1996; Johanson & Ahlberg, 2001; Shubin et al., 2006). However, homologous analyses of these body forms and structures in more ancient species have suggested that some of the morphologies related to vertebrate land dispersal were already present in early bony fish species. For instance, the presence of shoulder girdles on the articular surface of the endoskeleton in Late Lochkovian Psarolepis indicates that stem sarcopterygians already possessed an endoskeletal fin pattern similar to that of tetrapod stylopods (Zhu & Yu, 2009). In addition, primitive lungs, which originated from the respiratory pharynx and were located on the ventral side of the alimentary tracts, can be observed in several extant basal actinopterygians (bichirs, reedfish) and all extant sarcopterygians, as well as some fossils of coelacanths and salamanders (Cupello et al., 2017; Tissier et al., 2017) (Figure 1). This evidence suggests that, instead of relying on genetic innovations evolving after the first fish left their water habitat, this transition may have been accomplished by adopting physical traits and genetic components that already existed far earlier than when the transition occurred. Whether such an ancestral developmental regulatory network was present or not and how far this ancestral network can be traced in history are challenging questions for paleontologists. Three recent papers published in Cell provide new insights into this hypothesis. Wang et al. (2021) sequenced the giant genome of lungfish, the closest fish species to tetrapods, and Bi et al. (2021) sequenced the genomes of multiple early divergent ray-finned fish. Comparative genomic analyses from these two studies confirmed the presence of ancestral genetic regulatory networks that likely played essential roles in the development and evolution of various biological functions related to vertebrate land invasion. Although certain ancestral features have been lost in teleosts, the most derived fish lineage to evolve after whole-genome duplication (Sato & Nishida, 2010), they have been recreated in zebrafish by modifying their genetic makeup to reactivate the ancestral genetic network (Hawkins et al., 2021).