Chondrichthyes

Following the evolution of hinged jaws and paired pectoral/pelvic fins in Ordovician–Silurian stem-gnathostomes (placoderms and "acanthodians"), all living jawed vertebrates diverged during the Late Silurian (~425–430 Ma) into two sister superclasses, Chondrichthyes and Osteichthyes.

1. Chondrichthyes (Cartilaginous Fishes, ~1,280 living species): Comprising Elasmobranchii (sharks [Selachii] and skates/rays [Batoidea]) and Holocephali (ratfishes/chimaeras, such as Callorhinchus milii), which secondarily lost endochondral bone and macromeric dermal skull roofs while evolving a buoyant, tessellated prismatic calcified cartilage endoskeleton; and
2. Osteichthyes (Bony Vertebrates, >66,000 living species): Defined by endochondral bone replacement of cartilage, lepidotrichia fin rays, and an air-filled gas bladder or lung budded from the anterior gut, splitting immediately into Actinopterygii (Ray-Finned Fishes, ~35,000 species) and Sarcopterygii (Lobe-Finned Fishes and Tetrapods).

Although sharks and rays lack internal endochondral bone (having lost the secreted calcium-binding phosphoprotein, SCPP, gene cluster that drives osteoblast matrix mineralization in bony fishes, while retaining SCPP genes for placoid dermal denticles and conveyor-belt polyphyodont teeth), they are anything but primitive:

• Tesserae and Squalene Buoyancy: The hyaline cartilage of the chondrichthyan cranium, jaws, and vertebrae is wrapped in an outer mosaic of hexagonal hydroxyapatite tiles (tesserae) linked by collagen fibers, combining high compressive strength with shock-absorbing flexibility. Lacking a gas-filled swim bladder, pelagic sharks achieve near-neutral buoyancy in seawater through an enlarged liver (up to 25%–30% of body mass) saturated with low-density hydrocarbons—principally squalene (specific gravity 0.855 g/cm³) and diacylglyceryl ethers.
• Urea–TMAO Ureotelic Osmoregulation: Whereas marine teleost fishes are hypo-osmotic to seawater (~320 mOsm/kg vs. ~1,000 mOsm/kg) and constantly lose water across their gills, marine chondrichthyans (along with the coelacanth Latimeria) retain ~350–400 mM urea in their blood plasma to stay slightly hyper-osmotic to seawater (~1,050 mOsm/kg), excreting excess NaCl via a specialized rectal gland. To prevent 0.4 M urea from denaturing intracellular proteins, sharks co-accumulate ~180–200 mM trimethylamine N-oxide (TMAO) in a strict 2:1 urea-to-TMAO molar ratio: TMAO strengthens water-water hydrogen bonding and thermodynamically favors the compact folded state of proteins, exactly counteracting urea destabilization!
• Ampullae of Lorenzini (Nanovolt Electroreception) and the Slowest Vertebrate Genome: Derived from cranial lateral-line placodes, the ampullae of Lorenzini on the snout of sharks, rays, and chimaeras are jelly-filled canals lined with hair cells expressing Ca_V1.3 voltage-gated calcium channels and BK potassium channels that detect weak bioelectric fields down to 5 nanovolts per centimeter (5 nV/cm)—allowing a hammerhead shark or skate to locate a flatfish buried under sand solely from the bioelectric potential of its gill respiratory muscles. When Byrappa Venkatesh and colleagues (2014) sequenced the genome of the elephant shark (Callorhinchus milii, a holocephalan chimaera), they found that it has the slowest molecular substitution rate and most conserved synteny of any known jawed vertebrate—slower even than tetrapods or coelacanths.

A common misconception is that the air-breathing lungs of terrestrial tetrapods evolved from the hydrostatic swim bladder of ray-finned fishes. Comparative anatomy, paleontology, and developmental genetics prove the exact opposite—paired ventral lungs evolved first in the common ancestor of all Osteichthyes (~425 Ma), and the dorsal teleost swim bladder is a modified, dorsally shifted lung:

1. Basal Bichirs (Polypterus) Breathe Air with Paired Ventral Lungs: Sitting at the very base of Actinopterygii (sister to all other ray-finned fishes), African bichirs (Polypterus senegalus) possess paired lungs that bud from the ventral floor of the foregut, are supplied by paired pulmonary arteries branching off the sixth aortic arch, secrete pulmonary surfactant proteins (SP-A, SP-B, SP-C, SP-D) under Nkx2-1 control, and inhale atmospheric air through dorsal spiracles (homologous to the tetrapod middle-ear Eustachian tube!).
2. Migration from Ventral Respiratory Lung to Dorsal Hydrostatic Swim Bladder: Within Neopterygii, holostean gars (Lepisosteus) and bowfins (Amia) shifted the pneumatic duct to the dorsal roof of the esophagus while retaining heavily vascularized alveolar-like respiratory pockets for air gulping in hypoxic swamps. Finally, in Teleostei (and sturgeons), the dorsal air sac became the hydrostatic swim bladder—either retaining the esophageal pneumatic duct (physostomous in herrings, salmons, and carps) or losing the duct in adults and inflating/deflating the bladder internally via a countercurrent capillary rete mirabile and lactic-acid Root effect hemoglobin unloading in the gas gland (physoclistous in perches, cods, and reef acanthomorphs).

Why do Teleostei account for ~34,000 species (~50% of all living vertebrate species on Earth), whereas their sister clade Holostei (gars and bowfins) has only 8 living species?

1. The Teleost-Specific 3rd Round of Whole-Genome Duplication (Ts3R): Confirmed by whole-genome sequencing of the pufferfish (Takifugu rubripes), zebrafish (Danio rerio), and medaka (Oryzias latipes) by Axel Meyer, Yves Van de Peer, Sydney Brenner, and colleagues (1998–2007), the stem ancestor of all crown teleosts underwent a complete third round of whole-genome duplication (Ts3R) approximately 320–350 million years ago (followed ~80–100 Ma by an additional 4th round, Ss4R, in salmonids and cyprinid carps). Whereas mammals, birds, amphibians, coelacanths, and gars possess 4 Hox clusters (HoxA, B, C, D), zebrafish and medaka possess 7 Hox clusters (HoxAa, HoxAb, HoxBa, HoxBb, HoxCa, HoxCb, HoxDa), along with duplicated opsins, ion channels, pigment genes, and craniofacial regulators that underwent extensive subfunctionalization and cis-regulatory divergence.
2. Spotted Gar (Lepisosteus oculatus) as the Pre-Ts3R "Bridge Species": Because teleost genomes underwent rapid post-Ts3R gene loss, chromosomal rearrangements, and coding sequence acceleration, human disease enhancers are often undetectable when aligned directly against zebrafish (Danio rerio). In 2016, Ingo Braasch, John H. Postlethwait, and colleagues sequenced the genome of the spotted gar (Lepisosteus oculatus)—a non-teleost holostean fish that diverged before Ts3R—and discovered that the gar preserves entire 1-to-1 ancestral osteichthyan chromosomes and thousands of conserved non-coding regulatory enhancers shared with humans, acting as an indispensable evolutionary Rosetta Stone linking zebrafish genetics to human biomedical genomics.

How did teleost fishes decouple prey capture from chewing ("pharyngeal jaws")?

In basal actinopterygians and tetrapods, the oral jaws must simultaneously grasp prey and crush/swallow it. Crown teleosts—especially Euteleostei and Cichlidae (which radiated into >1,500 species across East African Great Lakes Victoria, Malawi, and Tanganyika in less than 10 million years)—evolved two biomechanical innovations: (1) cranial kinesis and upper-jaw protrusion, where depression of the lower mandible pulls via the maxillomandibular ligament on a mobile, tooth-bearing premaxilla to shoot the mouth forward as a high-velocity suction-feeding tube; and (2) pharyngeal jaws derived from modified fifth ceratobranchial gill arches in the throat, which crush snail shells or slice scales completely independently of the suction-specialized oral jaws.

Why do Antarctic icefishes (Channichthyidae) have crystal-clear, colorless blood with zero hemoglobin?

Inhabiting the freezing Southern Ocean (−1.9 °C, where cold water holds ~1.8× more dissolved O₂ than tropical water), the 16 species of Antarctic crocodile icefishes (family Channichthyidae, suborder Notothenioidei, such as Chaenocephalus aceratus) are the only known adult vertebrates that completely lack hemoglobin and red blood cells. As shown by H. William Detrich, Christina Cheng, and colleagues, the common ancestor of icefishes deleted the entire adult β-globin gene and the 5′ end of the α-globin locus. To survive on physically dissolved plasma oxygen alone, icefishes evolved a 4-fold larger blood volume, massive heart ventricles pumping at low viscosity, and antifreeze glycoproteins (AFGPs) evolved de novo from a duplicated pancreatic trypsinogen-like gene!

1. Venkatesh, B., Lee, A. P., Ravi, V., Maurya, A. K., Lian, M. M., Swann, J. B., ... & Warren, W. C. (2014). Elephant shark genome provides unique insights into gnathostome evolution. Nature, 505(7482), 174–179. doi:10.1038/nature12826
2. 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
3. Bi, X., Wang, K., Yang, L., Pan, H., Jiang, H., Wei, Q., ... & Zhang, G. (2021). Tracing the genetic footprints of vertebrate landing in non-teleost ray-finned fishes. Cell, 184(5), 1377–1391. doi:10.1016/j.cell.2021.01.046
4. Glasauer, S. M., & Neuhauss, S. C. (2014). Whole-genome duplication in teleost fishes and its evolutionary consequences. Molecular Genetics and Genomics, 289(6), 1045–1060. doi:10.1007/s00438-014-0889-2