Actinopterygii

Actinopterygii (from the Greek aktis, "ray," and pteryx, "wing" or "fin," commonly known as ray-finned fishes) is the largest and most ecologically diverse class of jawed vertebrates (Gnathostomata), comprising approximately 35,000 described extant species—accounting for more than 99% of all living fishes and roughly half of all living vertebrate species on Earth. Together with its sister superclass Sarcopterygii (lobe-finned fishes and tetrapods), Actinopterygii forms the clade Osteichthyes (bony vertebrates), which diverged from cartilaginous Chondrichthyes during the Late Silurian (~425–430 million years ago) as represented by early fossils such as Andreolepis, Guiyu, and the Devonian paleoniscoids Cheirolepis and Mimipiscis.

Whereas sarcopterygian paired fins contain a single monobasal humerus or femur articulated to a central muscular lobe of serial endoskeletal bones, actinopterygian paired pectoral and pelvic fins are webs of skin supported by parallel, segmented bony dermal rays (lepidotrichia) that articulate directly at their bases onto a row of short radial bones within the body wall, controlled by intrinsic muscles situated largely inside the trunk rather than down the length of the fin blade.

1. Dermal Scale Evolution (Ganoine to Elasmoid Cycloid/Ctenoid Scales): Early stem-actinopterygians and surviving basal lineages (bichirs and gars) armor their bodies with thick, rhomboidal, interlocking peg-and-socket ganoid scales topped with a glassy, multi-layered hypermineralized enameloid tissue called ganoine (secreted directly by the epidermis without an intervening mesenchymal layer) over vascularized dermal bone. During the Mesozoic radiation of Halecostomi (bowfin and Teleostei), this heavy ganoid armor was progressively thinned by eliminating the ganoine and spongy bone layers to produce lightweight, flexible, imbricated elasmoid scales—either smooth-margined cycloid scales (in salmon, herring, and carp) or comb-toothed ctenoid scales (in spiny-rayed acanthomorph perches and bass)—reducing hydrodynamic drag and body mass while increasing burst acceleration.
2. Transition from Respiratory Lungs to the Hydrostatic Swim Bladder: Comparative embryology and paleontology confirm that the last common ancestor of Osteichthyes possessed air-breathing lungs budded ventrally from the posterior pharynx (retained in Sarcopterygii and in the most basal living actinopterygians, the African bichirs and reedfish, Polypteriformes, which possess paired ventral lungs and drown if denied access to surface air!). In Actinopteri (sturgeons, gars, bowfin, and teleosts), this ancestral respiratory organ shifted dorsally above the digestive tract to become a single median gas bladder (swim bladder):
   • Physostomous Condition (in gars, bowfin, sturgeons, and basal teleosts such as salmon, trout, eels, and cyprinids): Retains an open pneumatic duct connecting the esophagus to the swim bladder, allowing the fish to gulp or burp air at the surface (and in Lepisosteus gars and Amia bowfin, to continue using the vascularized bladder as a bimodal air-breathing lung in hypoxic warm waters).
   • Physoclistous Condition (in derived spiny-rayed teleosts, Acanthomorpha): Closes off the embryonic pneumatic duct completely and regulates buoyancy at depth via a countercurrent capillary heat/gas exchanger—the rete mirabile and gas gland—which secretes lactic acid and CO₂ to trigger the Root effect (a pH-triggered drop in both the oxygen affinity and total O₂-carrying capacity of teleost hemoglobin), driving dissolved O₂ gas out of the blood into the swim bladder against hydrostatic pressures exceeding 100–400 atmospheres in the deep sea!
3. Evolution of Kinetic Premaxillary Jaw Protrusion and Pharyngeal Jaws:
   • In Paleozoic palaeoniscoids and living bichirs, the toothed maxilla was rigidly fused to the cheek bones (preopercle and infraorbitals), restricting the mouth to a simple wide-gaping scissor snap.
   • Across Holostei (Amia) and especially Teleostei (Acanthomorpha), the maxilla was freed from the cheek, lost its teeth, and was converted into a pivoting mechanical lever that pushes the toothed premaxilla rapidly forward (jaw protrusion) when the lower jaw drops—creating a tubular, high-velocity suction-feeding vortex that inhales elusive prey in <5 to 20 milliseconds while decoupling food capture (by the oral jaws) from food crushing and mastication (performed by a second set of toothed pharyngeal jaws derived from modified fifth gill arches in the throat, which enabled the explosive adaptive radiation of >1,700 species of East African Great Lakes cichlids and marine wrasses/parrotfishes!).

1. The Teleost 3R Whole-Genome Duplication and Subfunctionalization: Early in the evolutionary stem of Teleostei (Late Carboniferous–Early Permian, ~320–350 Ma), the ancestral genome underwent a third round of whole-genome duplication (TSGD / 3R, expanding the four gnathostome Hox clusters to seven or eight Hox clusters in zebrafish and medaka, followed by an additional fourth round, 4R, in salmonids and carps!). Through Duplication–Degeneration–Complementation (DDC / subfunctionalization) and neofunctionalization, duplicate teleost genes partitioned ancestral functions or evolved novel physiological roles:
   • For example, duplicating the skeletal muscle voltage-gated sodium channel gene SCN4A (Na_v1.4) into scn4aa and scn4ab allowed South American knifefishes and the electric eel (Electrophorus electricus) and African mormyrid elephantfishes to keep scn4ab in swimming muscle while mutating scn4aa exclusively in their modified muscle electric organs (enabling Electrophorus to discharge 600–860 volts without paralyzing its own swimming muscles, as shown by Harold H. Zakon et al., 2006!).
2. Antarctic Notothenioid Antifreeze Glycoproteins (AFGPs) and Icefish Hemoglobin Loss: In the freezing Southern Ocean (−1.86 °C, the freezing point of seawater), Antarctic notothenioid teleosts evolved two textbook genomic adaptations:
   • De Novo Evolution of Antifreeze Glycoproteins: As discovered by Arthur L. DeVries and Christina Cheng, notothenioids evolved secretory antifreeze glycoproteins (AFGPs) composed of tandem Thr–Ala–Ala tripeptide repeats conjugated to disaccharides from an ancestral pancreatic trypsinogen-like protease gene, which adsorbs onto nascent ice crystal prisms in the blood and depresses the hysteresis freezing point below −2.2 °C.
   • White-Blooded Crocodile Icefishes (Channichthyidae): The 16 species of Antarctic icefishes (Chaenocephalus aceratus, Chionodraco) are the only known adult vertebrates that completely lack red blood cells (erythrocytes) and hemoglobin (having deleted the entire β-globin gene and truncated the α-globin locus, while several species also lost cardiac myoglobin!). Surviving in oxygen-saturated, sub-zero Antarctic water via a 4-fold larger heart stroke volume, 2-to-4-fold greater blood volume, and wide low-resistance capillaries, icefishes carry all oxygen dissolved physically in colorless blood plasma.

Why was the spotted gar (Lepisosteus oculatus) genome so vital for connecting zebrafish genetics to human medicine?

Because zebrafish (Danio rerio), medaka, and pufferfishes (Takifugu rubripes) underwent the Teleost-Specific Whole-Genome Duplication (3R) followed by rapid sequence divergence and reciprocal gene loss, many human disease-associated non-coding cis-regulatory enhancers (CNEs) cannot be aligned directly between the human genome and the zebrafish genome. When Ingo Braasch, John H. Postlethwait, and colleagues (2016) sequenced the genome of the spotted gar (Lepisosteus oculatus)—a non-teleost holostean ray-finned fish whose lineage diverged just before the teleost 3R duplication—they found that the gar retains a conserved, non-duplicated karyotype (including whole-chromosome synteny with chicken and human chromosomes) and conserved non-coding enhancers that align directly to both human and zebrafish genomes, acting as a Rosetta Stone for functional comparative genomics.

How does the Weberian apparatus give freshwater carps, minnows, and catfishes (Ostariophysi) acute underwater hearing?

Whereas approximately 40% of marine fishes are spiny-rayed acanthomorphs, nearly 70% to 75% of all freshwater fish species on Earth belong to a single clade—Ostariophysi (comprising carps, minnows, zebrafish, characins/piranhas, catfishes, and electric knifefishes). Their evolutionary success in turbid rivers and lakes was driven by two coupled innovations: an epidermal alarm pheromone system (Schreckstoff / hypoxanthine-3-N-oxide) released when skin club cells are ruptured by a predator, and the Weberian apparatus—a chain of four tiny modified anterior vertebral bones (claustrum, scaphium, intercalarium, and tripus) that mechanically couple sound-induced volume oscillations of the gas-filled swim bladder directly to the perilymphatic sinus of the inner ear, acting as an underwater impedance-matching amplifier analogous to the three middle-ear ossicles of mammals!

1. Zakon, H. H., Lu, Y., Zwickl, D. J., & Hillis, D. M. (2006). Sodium channel genes and the evolution of diversity in communication signals of electric fishes: Convergent molecular evolution. Proceedings of the National Academy of Sciences, 103(10), 3675–3680. doi:10.1073/pnas.0600160103
2. Near, T. J., Eytan, R. I., Dornburg, A., Kuhn, K. L., Moore, J. A., Davis, M. P., ... & Smith, W. L. (2012). Resolution of ray-finned fish phylogeny and timing of diversification. Proceedings of the National Academy of Sciences, 109(34), 13698–13703. doi:10.1073/pnas.1206625109
3. Braasch, I., Gehrke, A. R., Smith, J. J., Kawasaki, K., Manousaki, T., Pasquier, J., ... & Postlethwait, J. H. (2016). The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons. Nature Genetics, 48(4), 427–437. doi:10.1038/ng.3526
4. Betancur-R, R., Wiley, E. O., Arratia, G., Acero, A., Bailly, N., Miya, M., ... & Ortí, G. (2017). Phylogenetic classification of bony fishes. BMC Evolutionary Biology, 17, 162. doi:10.1186/s12862-017-0958-3
5. Kim, B.-M., Amores, A., Kang, S., Ahn, D.-H., Kim, J.-H., Kim, I.-C., ... & Park, H. (2019). Antarctic blackfin icefish genome reveals adaptations to extreme environments. Nature Ecology & Evolution, 3(3), 469–478. doi:10.1038/s41559-019-0812-7