Non-teleost ray-finned fishes exhibit mosaic genomic features of lobe- and ray-finned fishes

A research team led by Prof. HE Shunping from the Institute of Hydrobiology (IHB) of the Chinese Academy of Sciences has discovered through genome sequencing that the non-teleost ray-finned fishes–bichir, paddlefish, bowfin and alligator gar–exhibit mosaic genomic features of lobe- and ray-finned fishes. The study was published in Cell.

The water-to-land transition during the Devonian is one of the most prominent events in vertebrate evolution. During this transition, various organs underwent adaptive changes, particularly those related to locomotion and respiration systems.

Rich fossil evidence suggests that many traits and functions related to this terrestrial evolution were present long before the ancestor of lobe- and ray-finned fishes appeared. Therefore, investigation of the genomes of extant species from early divergent lineages of ray-finned fishes may illuminate the genetic regulatory processes underlying trait evolution during the terrestrial transition.

The researchers produced a chromosome level assembly of the bichir (Polypterus senegalus), and draft genome assemblies for the American paddlefish (Polyodon spathula), the bowfin (Amia calva) and the alligator gar (Atractosteus spatula), which are representative species for each lineage of non-teleost ray-finned fishes.

The appearance of derived supporting appendicular structures was involved in the evolution of terrestrial locomotion, one of the major transitions in vertebrate evolution. Through comparative genomic analyses, the researchers found that early divergent lineages of ray-finned fishes exhibit many mosaic genomic features of lobe- and ray-finned fishes, particularly relating to regulatory elements for limb development.

The researchers then characterized olfactory receptor (OR) genes. Olfaction is important for vertebrate survival. Vertebrate genomes contain numerous OR genes, predominantly expressed in the olfactory epithelium of the nasal cavity. They found that non-teleost actinopterygians have mosaic OR features with a mixture of both types of OR genes, in accordance with the air-breathing characteristics of some species in these lineages.

To understand the evolution of lungs and their relationship to the swim bladders of fish, the researchers sequenced transcriptomes from 355 samples representing 10 tissues of eight vertebrate species. They confirmed that the lung and swim bladder are homologous organs, and discovered that functional lung-related genes are present in early ray-finned fishes.

In order to test the hypothesis that dominance of the conus arteriosus was an ancestral characteristic of the vertebrate cardiac outflow tract, the researchers functionally validated the essential role of a highly conserved element for cardiovascular development from a jawed vertebrate. The results implied that the ancestors of jawed vertebrates already had the potential gene networks for a cardio-respiratory system that could support air breathing.

The findings of this study are of great importance to understanding the water-to-land transition during vertebrate evolution since they clarify the genetic basis for limb development and for the respiratory system.


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